This paper presents 13 hypotheses regarding the specific behavioral abilities that emerged at key milestones during the 600-million-year phylogenetic history from early bilaterians to extant humans. The behavioral, intellectual, and cognitive faculties of humans are complex and varied: we have abilities as diverse as map-based navigation, theory of mind, counterfactual learning, episodic memory, and language. But these faculties, which emerge from the complex human brain, are likely to have evolved from simpler prototypes in the simpler brains of our ancestors. Understanding the order in which behavioral abilities evolved can shed light on how and why our brains evolved. To propose these hypotheses, I review the available data from comparative psychology and evolutionary neuroscience.

The neocortex performs a wide range of functions, including working memory, sensory perception, and motor planning. Despite this diversity in function, evidence suggests that the neocortex is made up of repeating subunits ("macrocolumns"), each of which is largely identical in circuitry. As such, the specific computations performed by these macrocolumns are of great interest to neuroscientists and AI researchers. Leading theories of this microcircuit include models of predictive coding, hierarchical temporal memory (HTM), and Adaptive Resonance Theory (ART). However, these models have not yet explained: (1) how microcircuits learn sequences input with delay (i.e., working memory); (2) how networks of columns coordinate processing on precise timescales; or (3) how top-down attention modulates sensory processing. I provide a theory of the neocortical microcircuit that extends prior models in all three ways. Additionally, this theory provides a novel working memory circuit that extends prior models to support simultaneous multi-item storage without disrupting ongoing sensory processing. I then use this theory to explain the functional origin of a diverse set of experimental findings, such as cortical oscillations.

Retracing the evolutionary steps by which human brains evolved can offer insights into the underlying mechanisms of human brain function as well as the phylogenetic origin of various features of human behavior. To this end, this article presents a model for interpreting the physical and behavioral modifications throughout major milestones in human brain evolution. This model introduces the concept of a “breakthrough” as a useful tool for interpreting suites of brain modifications and the various adaptive behaviors these modifications enabled. This offers a unique view into the ordered steps by which human brains evolved and suggests several unique hypotheses on the mechanisms of human brain function.

It has been suggested that the thalamus acts as a blackboard, on which the computations of different cortical modules are composed, coordinated, and integrated. This article asks what blackboard role the thalamus might play, and whether that role is consistent with the neuroanatomy of the thalamus. It does so in a context of Bayesian belief updating, expressed as a Free Energy Principle. We suggest that the thalamus-as-a-blackboard offers important questions for research in spatial cognition. Several prominent features of the thalamus—including its lack of olfactory relay function, its lack of internal excitatory connections, its regular and conserved shape, its inhibitory interneurons, triadic synapses, and diffuse cortical connectivity—are consistent with a blackboard role.Different thalamic nuclei may play different blackboard roles: (1) the Pulvinar, through its reciprocal connections to posterior cortical regions, coordinates perceptual inference about “what is where” from multi-sense-data. (2) The Mediodorsal (MD) nucleus, through its connections to the prefrontal cortex, and the other thalamic nuclei linked to the motor cortex, uses the same generative model for planning and learning novel spatial movements. (3) The paraventricular nucleus may compute risk-reward trade-offs. We also propose that as any new movement is practiced a few times, cortico-thalamocortical (CTC) links entrain the corresponding cortico-cortical links, through a process akin to supervised learning. Subsequently, the movement becomes a fast unconscious habit, not requiring the MD nucleus or other thalamic nuclei, and bypassing the thalamic bottleneck.

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