Wednesday, September 28, 2016

Peer Reviewed Article Explains How the Brain Works

I have been writing and fine-tuning this manuscript for ten years now and it is finally published. It outlines my model of working memory and my theory of how the brain and the mind are linked. They are linked by a very specific pattern of neural activity that creates the continuity of consciousness.

The open access article is titled:

"Incremental Change in the Set of Coactive Cortical Assemblies Enables Mental Continuity"

and can be read here for free:


This opinion article explores how sustained neural firing in association areas allows high-order mental representations to be coactivated over multiple perception-action cycles, permitting sequential mental states to share overlapping content and thus be recursively interrelated. The term “state-spanning coactivity” (SSC) is introduced to refer to neural nodes that remain coactive as a group over a given period of time. SSC ensures that contextual groupings of goal or motor-relevant representations will demonstrate continuous activity over a delay period. It also allows potentially related representations to accumulate and coactivate despite delays between their initial appearances. The nodes that demonstrate SSC are a subset of the active representations from the previous state, and can act as referents to which newly introduced representations of succeeding states relate. Coactive nodes pool their spreading activity, converging on and activating new nodes, adding these to the remaining nodes from the previous state. Thus, the overall distribution of coactive nodes in cortical networks evolves gradually during contextual updating. The term “incremental change in state-spanning coactivity” (icSSC) is introduced to refer to this gradual evolution. Because a number of associated representations can be sustained continuously, each brain state is embedded recursively in the previous state, amounting to an iterative process that can implement learned algorithms to progress toward a complex result. The longer representations are sustained, the more successive mental states can share related content, exhibit progressive qualities, implement complex algorithms, and carry thematic or narrative continuity. Included is a discussion of the implications that SSC and icSSC may have for understanding working memory, defining consciousness, and constructing AI architectures.

    1. Introduction

    The present article will delineate a simplistic but previously overlooked nonlinear dynamic pattern of brain activity. Two hypothetical constructs are introduced to describe this pattern. The first construct is state-spanning coactivity (SSC), which occurs when cortical nodes exhibit sustained coactivity during the span of short-term memory. The gradual evolution of SSC exhibits a distinctive spatiotemporal pattern of turnover as it plays out in real time. The second construct introduced here, incremental change in state-spanning coactivity (icSSC), refers to this pattern of turnover. icSSC conveys that the set of nodes that are simultaneously coactive changes incrementally as newly activated nodes are added and others are deactivated while a distinct subset remains in SSC. Spreading activity from the nodes in SSC select: 1) inactive neural nodes for activation, 2) active nodes for deactivation, and 3) active nodes for sustained activation. Because a distinct subset of nodes is always conserved from one brain state to the next, each state is embedded recursively in the previous state, amounting to an iterative process that has the potential to progress algorithmically toward a complex result. The general intention of the present article is to propose a qualitative model delineating the theoretical functions of SSC and icSSC from the perspective of cognitive neuroscience.

    The term SSC can be used either to denote a property or to designate a set of neurons. icSSC denotes a property or process ( Table 1). Both are related to the construct of working memory, which is defined as a system responsible for the transient holding and processing of attended information. The fundamental assumption made by this article is that the content of working memory can be said to be in SSC; and as working memory progresses over time, the content can be said to exhibit icSSC. This assumption is applied not only to working memory as the same could be said of attention, consciousness or short-term memory. icSSC can be taken to be the underlying neural substrate of mental continuity. As proposed here, mental continuity is a process where a gradually changing collection of mental representations held in attention/working memory emerges from the icSSC of neural nodes. The thematic and narrative quality created by this continuity during internally generated thought may be largely congruent with key facets of conscious experience. In the course of exploring how neural continuity creates mental continuity, this article will attempt to integrate current theoretical approaches while remaining consistent with prevailing knowledge.
    Table 1. Definition of key terms.

    Instantaneous coactivityThe coactivity of a set of cortical nodes in a single instant or state.

    State-spanning coactivity (SSC)

    Sustained coactivity exhibited by a set of two or more cortical nodes that spans two or more consecutive brain states.
    Incremental change in state-spanning coactivity (icSSC)

    The process in which a set of three or more neural nodes exhibiting SSC undergoes a shift in group membership, where at least two nodes remain in SSC and at least one is deactivated and replaced by a new node.

    Mental continuity

    The recursive interrelatedness of consecutive mental states made possible by icSSC.
    Animals are information-processing agents. They receive unprocessed data through sensory receptors, expose it to a massively parallel network of nodes and channels, and allow the interaction between the activity and the existing network to determine behavior. Even small invertebrates with elementary nervous systems exhibit ongoing, internally generated neural activity that temporarily biases the network weights. Because it involves mechanisms that include sustained firing, this continuous endogenous processing constitutes a fleeting form of SSC, even in animals like the nematode and fruit fly. In vertebrates, however, SSC involves the coactivation of high-level representations from long-term memory within a single, massively interconnected representational network (telencephalon). Each such representation is a record of the distribution of past neural activity corresponding to a recognizable stimulus or motor pattern. An instantaneous attentional state is composed of a novel combination of these template-like representations which together create contextual, cognitive content. The mammalian neocortex can hold a number of such mnemonic representations coactive for hundreds of milliseconds, using them to make predictions by allowing them to spread their activation energy together, throughout the thalamocortical network. This activation energy converges on the inactive representations in long-term memory that are the most closely connected with the current group of active representations, making them active and pulling them into SSC. Thus, new representations join the representations that recruited them, are incorporated into the set of coactive parameters in SSC and used in subsequent searches.
    When the activity of certain nodes can be sustained for several seconds at a time, as in primate association cortex, the complexity of search in such a system increases. Highly sustained activity allows prioritized representations to act as search parameters for multiple perception-action cycles. This permits more dynamic icSSC, whereby goal-relevant representations can be held constant as others are allowed to change. The icSSC taking place in association areas allows task-pertinent representations to be maintained over multiple cycles, in order to direct complex sequences of interrelated mental states. The individual states in a sequence of such states can be considered interrelated because they share representational content. The associations linking these sequences are saved to memory, impacting future searches and ultimately permitting semantic knowledge, planning, and systemizing.

    2. Sustained firing, attentional updating, and memory decay

    Mammals regularly encounter scenarios involving sets of stimuli that may remain present (or relevant) throughout the experience. In order to systemize such a scenario, it may be necessary to maintain mental representations of the pertinent contextual stimuli during the experience, and even afterward. Mammalian brains are well-equipped to do exactly this. The glutamatergic pyramidal neurons in the prefrontal cortex (PFC), parietal cortex, and other association cortices, are specialized for sustained firing, allowing them to generate action potentials at elevated rates for several seconds at a time [35]. In contrast, neurons in other brain areas, including cortical sensory areas, often remain persistently active for periods of mere milliseconds unless sustained input from either the environment or association areas makes their continued activity possible [35]. A neuron may exhibit tonic sustained firing due to temporary changes in the strength of certain synapses (short-term synaptic modification [80]), its intrinsic biophysical properties, extrinsic circuit properties (reverberatory circuits), or dopaminergic innervation [25]. Prolonged activity of neurons in association areas is largely thought to allow the maintenance of specific features, patterns and goals [8].

    Goldman-Rakic [37] and [38] first suggested that the phenomenon of sustained firing in the PFC is responsible for the information maintenance capabilities of the temporary storage buffers of working memory. Goldman-Rakic [39] also proposed that the PFC is parceled into several specialized regions, each of which is responsible for detecting, representing and sustaining a different extraction of multimodal information. Since then, the PFC, along with a number of association areas, has been divided into increasingly smaller modules, each with unique receptive/projective fields and functional properties including faculties such as short-term spatial memory, short-term semantic memory, response switching, error detection, reward anticipation, impulse suppression, and many others. Working memory, executive processing and cognitive control are now widely thought to stem from the active maintenance of patterns of activity in the PFC, especially the dorsolateral PFC, that correspond to goal-relevant features and patterns [33] and [34]. The temporary persistence of these patterns ensures that they continue to transmit their effects on network weights as long as they remain active, biasing ongoing processing, and affecting the interpretation of stimuli that occur during their episode of continual firing [57]. This persistence ensures that context from the recent past is taken into account during action selection.

    During any experience, some neural nodes exhibit more prolonged sustained firing than others. I will assume that in general the most enduringly active nodes correspond to what attention is most focused on, or the underlying theme that remains most constant as other contextual features change. From subjective introspection we know that when we envision a scenario in our mind's eye, we often notice it transform into a related but distinctly different scenario [46]. These two scenarios are related because our brain is capable of icSSC. In other words, the distribution of active neurons in the brain transfigures incrementally from one configuration to another, instead of changing all at once. If it were not for the phenomenon of icSSC, instantaneous information processing states would be time-locked and isolated (as in most serial and parallel computing architectures), rather than continuous with the states before and after them.

    These observations point to the notion that every cortical state is composed of a subset of elements from the previous state, and also composed of increasingly smaller subsets of elements of states directly before that. In fact, when comparing successive cortical states, the shorter the time difference between two states (on the order of seconds to fractions of milliseconds), the more similar in composition the two states will be. For instance, over the span of 10 milliseconds, a relatively large proportion of nodes will exhibit uninterrupted coactivity; however, over 10 s, this proportion will be much smaller. Here, we will be concerned with neural nodes exhibiting SSC at two distinct levels: A) short-term memory/priming, i.e., elements of long-term memory activated above baseline (for seconds to minutes); and B) the focus of attention/immediate memory, i.e., a small, perhaps more active subset of A (for milliseconds to a few seconds). Items in SSC within the focus of attention likely demonstrate active neural binding whereas items in SSC within short-term memory may not.
    Mental continuity and icSSC require a densely interconnected representational system such as a neural network that is capable of holding two or more representations (each specifying discrete and separate informational content) active over the course of two or more points in time (Fig. 1). The sustained activity of a single representation over time does not provide any context or associative/relational content, and so should not be taken to be sufficient for mental continuity. More than one representation is needed. Although its limits are presently being debated, the human neocortex is clearly capable of holding numerous representations active over numerous points in time.
    In Fig. 1 above, representations B, C, D, and E are active during t1, and C, D, E and F are active during t2. Thus representations C, D, and E demonstrate SSC because they exhibit continuous and uninterrupted activity from t1 through t2. The brain state at t1 and the brain state at t2 share C, D, and E in common and therefore can be expected to share other commonalities such as: similar information processing operations, similar memory search parameters, similar mental imagery, similar cognitive and declarative aspects, and similar experiential and phenomenal characteristics. The active nodes that have demonstrated SSC over any specific time interval can be thought of as constituting a unit with emergent functional properties. Together, these nodes impose sustained information processing demands on the lower-order sensory and motor areas within the reach of their long-range connections. The longer the activity in these higher-order neurons is sustained, the longer they remain engaged in hierarchy-spanning, recurrent (and reentrant) broadcasting throughout the cortex and subcortex.

    Compared to those of other mammals, human association areas contain more neurons, more intrinsic and extrinsic connections, and a higher capacity for sustained firing [33] and [34]. These characteristics presumably permit us to retain more information, for a longer time before it decays. This likely allows humans to better retain elements from recent thoughts, and allows the computational results of previous processes to more thoroughly inform subsequent ones. This once influenced the present author to assume that somehow thoughts are “longer” in humans than they are in other animals; however, if thought has an architectural geometry marked by length, then mustn't it also have starting and stopping points? If persistent activity of individual representations in SSC is staggered and overlapping, then there cannot be objective stopping or starting points of thought. Instead, thought itself must be composed of the startings and stoppings of huge numbers of individual elements that could be depicted graphically in the form of a continuous, stream-like distribution (Fig. 2). Therefore, it is not that human thoughts are somehow longer than in other animals; rather, human thought is composed of larger sets of representations that are capable of remaining coactivated longer [70] and [71].
    The reallocation of processing resources in Fig. 2 is similar to the behavior of treads on a military tank. Individual treads are continually placed on the ground temporarily, and the treads that have sat on the ground for the longest are withdrawn in series. The total set of treads touching the ground in one moment partially overlaps with the total set in the next. Our mental set of active representations may cycle in an analogous, although more flexible and stochastic manner. A more precise analogy and schematic will be introduced in Section 5.
    PFC neurons are likely tuned throughout life to best determine what aspects of the present environment should be maintained in SSC (or released from maintenance) given the current scenario and its preceding circumstances. When confronted with a complex configuration of stimuli, the PFC may select the representations that it “predicts” should be temporarily maintained for their processing utility in the immediate future. This selection process is likely determined by the incoming stimulus configuration itself, prior probability as encoded in the network, and the network-biasing representations already in SSC. Initially during development, the process of selecting neurons for persistent activity may be random and heavily influenced by innate connectivity. The expertise of the PFC is probably garnered slowly, over developmental time, after connections between groups of neurons exhibiting sustained firing are strengthened for their role in mediating task proficiency and reward achievement. The selection process for SSC is perhaps best exemplified by the ability to identify and maintain strategically important representations from a forthcoming scenario. A sentence (spoken or written) is a suitable example. A sentence will be comprehended if: 1) the relevant representations are identified and enter into SSC; 2) all the necessary representations are sustained throughout the duration of the sentence; 3) the network has enough experience with this particular combination of representations to build the appropriate imagery, depicting them in the way they were intended. Most people have had the experience where either the wrong representations were anchored upon, or the right representations could not be maintained for long enough, and the sentence had to be repeated or reread.

    The quantity of SSC can be thought of as directly proportional to the number of sustained nodes and the average length of time of their activity [69], [70] and [71]. It should also be possible, in theory, to quantify icSSC by determining the proportion of previously active neural nodes that have remained active over a given time period. One way to do this would be to determine how long it takes half of the currently firing association neurons to sufficiently reduce their firing. Employing the idea of a “half-life” may be a useful concept even though the “decaying quantity” may not exhibit constant exponential decay, and despite the fact that current scanning and recording methods could not produce the necessary data without significant extrapolation. If the average rate of decay was properly operationally defined and could be measured, then cognitive neuroscientists would be able to discuss the “icSSC half-life” associated with individuals or even species. Would it be informative if it were found that Wistar rats have an average icSSC half-life of, say, one second, macaque monkeys twice this and humans twice that? Even in a single individual, this number is likely to vary depending on the task at hand, level of arousal, motivational state, brain oscillation factors, and brain regions assayed. Moreover, short-term memory/priming would have a much longer half-life than the focus of attention. An SSC/icSSC profile featuring numerous such assays could be computed for an individual based on various standardized criteria. If characterized correctly and averaged meaningfully, these numbers could prove to be consistent and reliable psychometric markers. Tononi [83] developed a method for calculating a measure of “integrated information” within a single, static brain state. The concept of icSSC could be used to expand on this measure in order to calculate the integration of information between two brain states, or across multiple brain states.

    It is not always the case that the majority of representations are conserved from one thought to the next. When they become a lower priority, nearly all items in the focus of attention can be displaced at the same time. This readily happens when we are exposed to a new, salient, perhaps emotionally laden stimulus. Whenever a person loses their train of thought, and forgets what they were just thinking, SSC in the focus of attention (though not necessarily in short-term memory) is interrupted. SSC “jumps,” reallocating attentional resources, and reorienting to the new stimulus configuration and its accompanying set of features. Such a jump would constitute a disruption of, or fluctuation in, mental continuity. The degree of fluctuation in continuity varies depending on the proportion of neural activity that is abruptly deactivated (Fig. 3). Because icSSC is the change in SSC, as attention shifts, SSC decreases, and icSSC increases.
    In the most intelligent mammals, late motor output and early sensory activity are heavily influenced by several seconds of sustained input from association areas. In mammals with smaller association areas, capable of less SSC, motor and sensory output are informed by a much briefer window of continuous activity. High SSC likely allows “behavioral continuity” where sequential behaviors can be complexly interrelated and mutually informed. This can be contrasted with the more isolated and impulsive behaviors seen in individuals with injuries to the PFC (i.e., field-dependent behavior in which the patient's behavior is dictated by incidental cues and distractions). In fact, the temporal extent of SSC may be a major facet of the “general factor” of intelligence. SSC may be related to, and a primary determinant of, attention span, behavioral flexibility, working memory capacity, short-term memory capacity, reasoning ability, and general fluid intelligence. Furthermore, significant individual differences in SSC may exist in humans where deficits in this capacity may map onto a variety of clinical syndromes such as schizophrenia, mental retardation, cognitive aging, chronic stress, various forms of intoxication, and prefrontal injury. Nevertheless, why did SSC and icSSC evolve, what purposes do they serve, and how do they relate to dopaminergic functions? Mammals most likely evolved the capacity to sustain certain representations so that hypothetical groupings of representations could be modeled and systemized.

    Thursday, August 18, 2016

    Chronic Stress Adaptively Remodels the Cortex and Hippocampus

    In a new article published by Behavioral Processes I describe how the effects of chronic stress on the brain may be evolutionarily selected. The full open-access article can be found here:

    Chronic Stress, Cortical Plasticity and Neuroecology


    Prolonged psychological stress and accompanying elevations in blood cortisol are known to induce hypometabolism and decreasing synaptic density in the hippocampus and the prefrontal cortex (PFC). This article evaluates and explores evidence supporting the hypothesis that these, and other, selective effects of prolonged stress constitute a neuroecological program that adaptively modifies behavior in mammals experiencing adverse conditions. Three complementary hypotheses are proposed: 1) chronic stress signifies that the prevailing environment is life-threatening, indicating that the animal should decrease activity in brain areas capable of inhibiting the stress axis; 2) stress signifies that the environment is unpredictable, that high-level cognition may be less effective, and that the animal should increase its reliance on defensive, procedural and instinctual behaviors mediated by lower brain centers; and 3) stress indicates that environmental events are proving difficult to systemize based on delayed associations, and thus the maintenance of contextual, task-relevant information in the PFC need not be maintained for temporally-extended periods. Humans, along with countless other species of vertebrates, have been shown to make predictive, adaptive responses to chronic stress in many systems including metabolic, cardiovascular, neuroendocrine, and even amygdalar and striatal systems. It is proposed in this article that humans and other mammals may also have an inducible, cerebrocortical response to pronounced stress that mediates a transition from time-intensive, explicit (controlled/attentional/top-down) processing of information to quick, implicit (automatic/preattentive/bottom-up) processing.

    Keywords: cortisol, evolution, executive control, hippocampus, neuroecology, prefrontal cortex, stress cascade, top-down processing

    1.0  Chronic Stress, Cortical Plasticity and Neuroecology

    Organisms throughout the five kingdoms retain certain capacities to adaptively modify their phenotype in order to better conform to their environment (Auld et al., 2010). Some of these changes are transient and reversible, whereas some are comprehensive and permanent. The studies of phenotypic plasticity, polyphenism and “predictive, adaptive responses” have shown that virtually all species can be reprogrammed by portending environmental cues, that the morphological changes are brought about by alterations in gene expression, and that the changes allow conformation to occasional but regularly recurring environmental pressures (DeWitt & Scheiner, 2004). These alternate environments typically involve stressors which demand different body types, behaviors, reproductive tactics, and life-history strategies (Pigliucci, 2001). Often the adaptive response to stress is conserved within groups of closely related organisms that inhabit similar ecological niches (Via & Lande, 1985). For instance, even though all organisms respond plastically to nutrient/energy deprivation, mammals exhibit a unique suite of physiological changes aimed at lowering the metabolism of specific organ systems in the interest of continued survival (Wells, 2009). This article discusses phenotypic changes in mammalian brain structure and neurochemistry, known to be largely mediated by alterations in gene expression, that occur in response to chronically high levels of the stress hormone cortisol. Herein, well-documented brain changes, and their behavioral correlates, are characterized as potentially adaptive responses to adverse ecological scenarios. Different lines of converging evidence will be considered in an exploratory and expository manner.

    The mature mammalian brain can be reshaped by chronic or prolonged stress in two primary ways: 1) metabolic activity, dendritic growth and implicit memory are enhanced in the amygdala and caudate nucleus; and 2) metabolic activity, dendritic growth, explicit memory and inhibitory functions are reduced in the hippocampus and prefrontal cortex (PFC) (Cohen et al., 2007; Sapolsky, 2003). Many of the effects of stress on neural circuitry are mediated by the stress hormone cortisol which activates the numerous cortisol receptors present in the amygdala, hippocampus, and PFC (Morales-Medina et al., 2009). Once activated, these receptors trigger pathways that result in the expression or silencing of particular genes, which are the molecular antecedents thought to be responsible for a large proportion of the neurological remodeling (Petronis, 2000, 2004; DeWitt & Scheiner, 2004). This remodeling, much of which has been shown to be epigenetic, may help stressed mammals to adapt to environmental adversity, with its particular set of recurrent and ecologically relevant threats and opportunities.

    In the literature, the responses to stress in the amygdala and basal ganglia have been attributed adaptive significance (Sapolsky, 2003), but the responses of the hippocampus and PFC have mostly eluded the attention of evolutionary biologists (Reser, 2007). Increased activity in the amygdala is thought to help animals become more sensitive and responsive to threat (Radley & Morrison, 2005). Neural and dendritic hypertrophy in the basolateral amygdala potentiates the mechanisms dedicated to identifying stressors, and mobilizing the body to address them (Sapolsky, 2003). The amygdala stimulates the paraventricular nucleus of the hypothalamus (PVN) to release stress hormones, and hypertrophy of the amygdala increases its capacity to do this (Roozendaal et al., 2009). A different way to potentiate activity in the amygdala is to release it from the structures that tonically inhibit it (Mitra & Sapolsky, 2008). The PFC and hippocampus have long been identified in neurology as brain regions capable of inhibiting the autonomic and emotional responses to fear-inducing stimuli (Cannon, 1929; Papez, 1937; MacLean, 1949; see LeDoux, 1987, for a review). This circuitry ensures that mammals can override the fear response if they make the determination that the stimulus may appear threatening but is not actually threatening (Morgan et al., 1993). Diminishment of activity in the PFC and hippocampus may ensure that the areas that incite stress, the amygdala and PVN, can function unimpeded during stressful times.

    Decreased activity in the PFC and hippocampus may also adaptively influence the animal to be less cerebral and more impulsive (Reser, 2007). When facing lasting adversity, it may be advantageous to suppress the PFC and hippocampus because these areas put inhibitory pressure on defensive, instinctual, and dominant responses. When an animal experiences extreme stress, it is probable that its high-order behavioral strategies are proving relatively ineffectual (Boonstra, 2005). It may benefit such an animal to be less reliant on learned behavior, and more reliant on genetically programmed and species-specific behaviors. Hence, the changes in the hippocampus and PFC may protectively disinhibit innate and instinctual urges (Reser, 2007).

    The present article will elaborate on three complementary hypotheses: 1) stress signifies that the prevailing environment is antagonistic, and that the animal should not suppress the stress response or inhibit conditioned fears; 2) stress signifies that behaviors that the animal has learned may be inefficacious or deleterious and that it should increase its reliance on innate behaviors over learned behaviors; and 3) stress indicates that environmental events are proving difficult to systemize on long time scales (using delayed associations) and thus the maintenance of contextual, task-relevant information in the PFC need not be maintained for temporally-extended periods.

    Several neurological changes to areas including the amygdala, the caudate nucleus, the hippocampus, the mPFC, and the PFC in general will be discussed. Table 1 describes the general psychological consequences of these changes, the implications that they have for modern people as well as hypothetical implications that they may have had for prehistoric foragers. This table attempts to highlight the disparity between the limiting repercussions of these changes in the modern “information age” and their potentially adaptive significance in the prehistoric past.

    Table 1

    The Neurological Effects of Stress, Then and Now

    Neurological State
    Psychological Consequences
    Implications for Moderns
    Implications for Foragers
    Amygdala hyperactivity
    Potentiation of conditioned fears
    Anxiety, fear and excessive stress
    Healthy caution, preparedness and mobilization
    Caudate hyperactivity
    Potentiation of procedural or habitual movements
    Intrusion of habitual or procedural responses
    Increased reliance on movements that have been proven effective
    PFC hypoactivity
    Behavioral disinhibition
    Working memory and goal-setting problems
    Increased reliance on instinctual and appetitive impulses
    mPFC hypoactivity
    Impaired inhibition of conditioned fears
    Exaggerated stress responses to nonfatal threats
    Enhanced awareness of potential threats
    Hippocampal hypoactivity
    Inaccessibility of contextual and episodic information
    Explicit/ declarative memory problems
    Increased reliance on dominant and procedural responses

    Interestingly, prenatal and early-life stress cause a pattern of changes that is strikingly similar to the changes that occur in response to chronic stress in adulthood (Weinstock, 2008). When pregnant rodent or primate mothers are stressed, they program highly analogous changes in the amygdala, hippocampus, and PFC of their offspring (Francis et. al., 1999; Kapoor et al., 2006; Schneider et al., 1999). The behavioral changes in these offspring, which include increased vigilance, fearfulness and stress responsivity, have been interpreted by Michael Meaney and colleagues as constituting a predictive and adaptive response to early environmental adversity (Zhang et al., 2006). In this interpretation the amygdalar changes are attributed adaptive qualities. However, the role of the hippocampus and the PFC in contributing to this behavioral response has been neglected. Moreover, psychiatric disorders such as anxiety, depression, posttraumatic stress disorder and schizophrenia are associated with prenatal and postnatal stress, and involve the same pattern of changes to the hippocampus, PFC and amygdala (Axelson, 1993; Corcoran, 2001).

    Elevated levels of noradrenaline and dopamine, such as occur during acute yet transient stress, impair PFC and hippocampus-dependent abilities such as working memory and attention regulation, but strengthen amygdala, caudate and subcortical-dependent functions such as fear conditioning, habitual behaviors and reflexes (Elliot & Packard, 2008; Packard & Teather, 1998). Thus, acute stress, chronic stress, prenatal stress and a number of major psychiatric disorders have all been shown to engineer a switch from thoughtful “top-down” control based on task-relevance to bottom-up control based on salience (Buschman & Miller, 2007; Hermans et al., 2014). This article focuses on these cortical corollaries of pronounced stress, and attempts to interpret them in terms of their ecological utility to mammals, from wild rodents to prehistoric humans. If the neurological changes that respond to stress were diffuse or only degenerative this might indicate that they do not represent adaptation. That the alterations are very selective, that they completely spare critical cortical and subcortical regions, that there are dozens of documented molecular pathways that converge toward these changes (Stankiewicz et al., 2013), and that arborization and neural activity in the amygdala (Francis et al., 1999; Radley & Morrison, 2005; Vyas et al., 2003) and caudate (Kim et al., 2001; Schwabe et al., 2008) is actually enhanced, suggests that these changes may not be pathological. To further explore the proposed evolutionary rationale for why these changes, in adulthood and in utero, might constitute an adaptive response we turn to the neurobiology of stress perception.

    The rest of the article can be found here:

    Here are some passages from an earlier version of the manuscript that I removed:

    The PFC and hippocampus are probably targeted by the stress cascade because of their subtle contributions to behavior. They are both multimodal convergence areas that integrate information from multiple sensory areas to allow sensory reconciliation and ultimately self-control and self-guided action. These two areas do not control any basic unitary ability though. Most other areas of cortex, if rendered hypometabolic, would result in the loss of motor skills, or sensory processing. For instance, pronounced dendritic shrinkage in the occipital lobe would adversely affect or even abolish certain visual abilities. Yet the neuropathology in the stress cascade spares early sensory areas and even most association areas and is confined to the more expendable, more abstract areas...

    Cortical dendritic spines are highly motile structures that are capable of responding quickly to physiological and environmental input - responses that are integral to learning and behavioral plasticity (Kirov et al., 2004). Restricting their growth and actually retracting them should limit behavioral plasticity and also reduce the accessibility of information (memories) that is encoded by the synaptic weights. That the apical, but not the basal dendrites are affected (Brown et al., 2005) suggests that this response is designed to reduce the contribution of higher cortical layers. The superficial layers, II and III, are responsible for sending and receiving recurrent (feedback/ topdown/ modulatory) signals that encode subtle distinctions of learned information (Calvin, 1995). This epigenetic program spares the lower layers which receive inputs from and produce outputs to subcortical areas. Such apical degeneration could make it so that cortical areas are accessible to lower areas, only they are being used to a lesser extent. In other words, during stress it is still important to draw vertically from various cortical columns, or clusters of cells with similar receptive fields, however; it is less important to draw from the higher cortical lamina (layers II and III). This makes the content of memories accessible, but minimizes the horizontal cross-talk within higher layers, perhaps resulting in simplified answers to behavioral questions. It emphasizes bottom up at the expense of top down processing. Cognition without the horizontal information-sharing decreases the temporal persistence of information processing, potentially contributing to the documented diminishments in working memory and inhibition. It should be very interesting to better resolve how the debranching of apical dendrites affects the processing within and between individual cortical columns...

    The dendritic changes in the medial PFC follow another definite pattern where larger spines are affected to a greater extent. Larger dendritic spines which are less plastic, have larger synapses, a high proportion of AMPA receptors, are stable, and are thought to represent “memory spines” (Kasai et al., 2003). Small spines are more plastic, labile, have smaller synapses with a high proportion of NMDA receptors, and can either retract or become larger and stable and these are thought to represent “learning spines.” During stress the larger spines are the ones that retract the most (Cerqueira et al., 2007), hence it should be interesting to determine how this affects the cell’s receptive field, and why. Clearly there is a biological favoritism here. It should be important to understand why larger spines should retract. This seems to be consistent with the second hypothesis described in the introduction, suggesting that stress signifies that learned behavior may be ineffectual, and that the animal should increase its reliance on instinctual and procedural behaviors...

    Perhaps the stress cascade makes an animal hesitant to stray far from home to keep it safe. And perhaps it also makes it so that the animal’s inclination to go out and explore, to be an infovore and search out new areas, because it has mastered the old ones, is diminished.

    It will be interesting to see how reflexes are potentiated by stress aside from hyperactivity in the caudate nucleus. I imagine that it is possible that the corticospinal system (which is controlled by the frontal cortex) is downregulated relative to the extrapyramidal motor systems. It is possible that the primary motor cortex (which commands the cortiospinal (pyramidal) system is unchanged but the areas that regulate and inhibit its activity (like the premotor, supplementary motor and presupplementary motor areas) are downregulated. In fact, the presupplementary motor cortex but not the primary motor cortex is damaged in schizophrenia. This means that stress makes you worse at planning complex sequences of movements.

    The stress cascade acts to reduce the amount of information that individuals take with them through time. The PFC generally learns to pick out key stimuli from different scenarios  The more stressed an animal has been the fewer elements of its immediate past can be recalled attentively and applied to the current situation. Animal species that have been endowed with large working memories by evolution can expect that it will be helpful to have many brain areas, corresponding to the last several seconds of thought (or experience), primed at once so that they may bring elements of their immediate past to bear on the present. Less intelligent animals can take only the most salient aspect with them through time, and old, hardwired or subcortical areas are what programs most of their actions in the present.

    Many animals, such as a large proportion of invertebrates, that inhabit simple ecological niches have very simple nervous systems and come into the world with nearly all of the behavior needed preprogrammed into their bodies by their genes. These animals can only learn very rudimentary things that only slightly modify their innate systems. As brain to body ratio and encephalization have increased in the animal kingdom, over the last 700 million years, many species have been granted increasing autonomy over their own behavior. More intelligent animals, like those in our phylum, chordates, have the ability to be programmed by the environment so that the behavior of any two individuals of the same species may be very different especially if they developed in differing environments.

    The mammalian cortex, which is highly developed in humans, allows very high degrees of behavioral plasticity for planned actions (Moscovich, 2007). Such a high degree of self-government and freedom from instinct would potentially be very dangerous for animals such as reptiles, amphibeans and fish because they would probably often be hard pressed to develop adaptive behaviors on their own. A vastly increased ability for new learning probably developed in mammals because of the presence of maternal care and instruction. Developing mammals were unique because they had doting models from whom to learn memes. But what if a young mammal’s learning does not lead to adaptive behavior and the mother’s own stress detracts from her ability to share knowledge? Might it then be beneficial to return to instinctive behavior? If natural selection could have accomplished it, it probably would have given mammals the connections needed at birth to live, eat and procreate as it does in very simple invertebrates. Mammalian ecological niches are so variable though, that genes could never prepare them properly by preprogramming all of their behavior. For this reason higher cognitive areas are a necessity although perhaps a calculated risk.

    People cite many reasons for what pressures caused the human brain to evolve: complex foraging techniques, hunting, social abilities, Machiavellian intelligence. I think that a major contributor to the evolution of human intelligence was the stress free period that resulted from the manufacture of weapons. Intelligence evolved because hominids in our direct line of descent (that we descended from lower forms is ironic) evolved to hunt in groups and fashion weapons, this increased order and decreased predation (intraspecies aggression probably stayed the same after weapons). Now that the world was safer, people had time to see order. The abilities to think things all the way through and to plan ahead were selected. The ability for self discipline and to exercise control over wants was selected for. The ability to do the harder thing and to hold out or to plan, to set things up in advance and “wait for it to be a sure thing.” Sometimes newly appreciated phenomena give us a new vantage point to see other things. I think that the stress cascade gives us valuable insight into the evolution of human intelligence and tells us that safety and order, allowed us time to deliberate which allowed selection to act on the other cognitive theories like hunting, social abilities and such. The way that you think about the things in your environment determines what you extract from them. It seems likely that, like with most other traits, there might be crucial genetic variations that ended up causing an aneurotypical way to think about or perceive the environment. ADHD, depression, PTSD and anxiety may all represent different but similarly adaptive ways to extract specific information from a presumed adverse environment. The predictive adaptive response of the stress cascade made the dangerous expansion of the human mind, not so dangerous.

    Perhaps only a minority of people are neurologically well suited for occupations that demand cognitive rigor, planning, foresight and intense concentration. Since there was no electrical engineering, computer programming or rocket science in the ancestral past, sometimes it is unclear how these skills were selected for during human evolution. Perhaps neurological dispositions like these represent an optimistic outlook that expects a systemizable and orderly environment. Delayed gratification, marshmallow studies, waiting longer means more intelligence and school performance. Tie between adversity and delay. Only in a good environment can you delay. The brain evolved to learn about the things that we are motivated about. Today we learn about things that have nothing to do with survival. Hominids probably would have found it hard to get motivated about school work and occupational expertise but would have stayed interested in activities that lead directly to food, shelter and social interaction. And this would have been good for them.

    The discipline of behavioral ecology is based on the premise that cognitive traits and the neural substrates responsible for them are shaped by natural selection and hence are fine tuned to respond to the traditional environment of the species in question. A subdivision of this discipline, called neuroecology, attempts to draw causal links from variations in brain structure between species to the lifestyle of these species. For instance, a species that forages over wide terrain or hides (caches) food more than a similar species would be expected to have a larger hippocampus because the hippocampus, an area responsible for spatial cognition, plays a bigger role in its ecological behavior. Neuroecology has received some criticism because the predictions that it tests are largely adaptationist (i.e. if it exists it must have been naturally selected) but since has been largely redefined.

    Reality testing of past memories is difficult for one main reason, because the semantic aspects of a memory can be completely isolated from the contextual. The way that we test a memory, to see if it was imagined or not, is to try to recollect the context. I have a strong memory that my friend misheard a song lyric in a popular song. The friend heard “she is a Swedish drum” and the lyric is “she is the sweetest drug.” I asked my friend about this over a year later and my friend denied it completely. I knew that it took place and I scoured my memory… and got no where. All I could remember was that the event took place, but I had no contextual cues. I can’t remember where we were, what else we were saying, what time of day it was, or if I was alone daydreaming the scenario to life. The only other thing I could remember, besides the literal lyrics, was that it was a real memory, is this really trustworthy though? Could the “this was real” memory actually just be a mutated “wouldn’t it be funny if this had been real” memory? Maybe if it all comes back really FAST, then this indicates that it is hippocampal and thus veridical in origin. If it comes back more slowly, it could be confabulated or reconstructed.