No relative expansion of the number of prefrontal neurons in primate and human evolution

Human evolution is widely thought to have involved a particular expansion of prefrontal cortex. This popular notion has recently been challenged, although controversies remain. Here we show that the prefrontal region of both human and nonhuman primates holds about 8% of cortical neurons, with no clear difference across humans and other primates in the distribution of cortical neurons or white matter cells along the anteroposterior axis. Further, we find that the volumes of human prefrontal gray and white matter match the expected volumes for the number of neurons in the gray matter and for the number of other cells in the white matter compared with other primate species. These results indicate that prefrontal cortical expansion in human evolution happened along the same allometric trajectory as for other primate species, without modification of the distribution of neurons across its surface or of the volume of the underlying white matter. We thus propose that the most distinctive feature of the human prefrontal cortex is its absolute number of neurons, not its relative volume.

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Determinants of functional synaptic connectivity among amygdala-projecting prefrontal cortical neurons

10.1101/2021.11.07.467611 ◽

2021 ◽

Author(s):

Yoav Printz ◽

Pritish Patil ◽

Mathias Mahn ◽

Asaf Benjamin ◽

Anna Litvin ◽

...

Keyword(s):

Prefrontal Cortex ◽

Cortical Neurons ◽

Large Scale ◽

Basolateral Amygdala ◽

Local Network ◽

Synaptic Connectivity ◽

Synaptic Organization ◽

Intrinsic Properties ◽

Subcortical Structures ◽

Prefrontal Cortical

The medial prefrontal cortex (mPFC) mediates a variety of complex cognitive functions via its vast and diverse connections with cortical and subcortical structures. Understanding the patterns of synaptic connectivity that comprise the mPFC local network is crucial for deciphering how this circuit processes information and relays it to downstream structures. To elucidate the synaptic organization of the mPFC, we developed a high-throughput optogenetic method for mapping large-scale functional synaptic connectivity. We show that mPFC neurons that project to the basolateral amygdala display unique spatial patterns of local-circuit synaptic connectivity within the mPFC, which distinguish them from the general mPFC cell population. Moreover, the intrinsic properties of the postsynaptic mPFC cell and anatomical position of both cells jointly account for ~7.5% of the variation in probability of connection between mPFC neurons, with anatomical distance and laminar position explaining most of this fraction in variation. Our findings demonstrate a functional segregation of mPFC excitatory neuron subnetworks, and reveal the factors determining connectivity in the mPFC.

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Lateral prefrontal cortex: architectonic and functional organization

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2005.1631 ◽

2005 ◽

Vol 360 (1456) ◽

pp. 781-795 ◽

Cited By ~ 672

Author(s):

Michael Petrides

Keyword(s):

Prefrontal Cortex ◽

Functional Organization ◽

Macaque Monkey ◽

Primate Species ◽

Comparative Approach ◽

Fine Motor ◽

Precentral Gyrus ◽

Control Processes ◽

Dorsolateral Prefrontal ◽

Prefrontal Region

A comparison of the architecture of the human prefrontal cortex with that of the macaque monkey showed a very similar architectonic organization in these two primate species. There is no doubt that the prefrontal cortical areas of the human brain have undergone considerable development, but it is equally clear that the basic architectonic organization is the same in the two species. Thus, a comparative approach to the study of the functional organization of the primate prefrontal cortex is more likely to reveal the essential aspects of the various complex control processes that are the domain of frontal function. The lateral frontal cortex appears to be functionally organized along both a rostral–caudal axis and a dorsal–ventral axis. The most caudal frontal region, the motor region on the precentral gyrus, is involved in fine motor control and direct sensorimotor mappings, whereas the caudal lateral prefrontal region is involved in higher order control processes that regulate the selection among multiple competing responses and stimuli based on conditional operations. Further rostrally, the mid-lateral prefrontal region plays an even more abstract role in cognitive control. The mid-lateral prefrontal region is itself organized along a dorsal–ventral axis of organization, with the mid-dorsolateral prefrontal cortex being involved in the monitoring of information in working memory and the mid-ventrolateral prefrontal region being involved in active judgments on information held in posterior cortical association regions that are necessary for active retrieval and encoding of information.

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Common coding of expected value and value uncertainty memories in the prefrontal cortex and basal ganglia output

Science Advances ◽

10.1126/sciadv.abe0693 ◽

2021 ◽

Vol 7 (20) ◽

pp. eabe0693

Author(s):

Ali Ghazizadeh ◽

Okihide Hikosaka

Keyword(s):

Prefrontal Cortex ◽

Basal Ganglia ◽

Cortical Neurons ◽

Expected Value ◽

Common Coding ◽

Repetition Suppression ◽

Free Viewing ◽

Gaze Bias ◽

Single Unit Recordings ◽

Value Preferences

Recent evidence implicates both basal ganglia and ventrolateral prefrontal cortex (vlPFC) in encoding value memories. However, comparative roles of cortical and basal nodes in value memory are not well understood. Here, single-unit recordings in vlPFC and substantia nigra reticulata (SNr), within macaque monkeys, revealed a larger value signal in SNr that was nevertheless correlated with and had a comparable onset to the vlPFC value signal. The value signal was maintained for many objects (>90) many weeks after reward learning and was resistant to extinction in both regions and to repetition suppression in vlPFC. Both regions showed comparable granularity in encoding expected value and value uncertainty, which was paralleled by enhanced gaze bias during free viewing. The value signal dynamics in SNr could be predicted by combining responses of vlPFC neurons according to their value preferences consistent with a scheme in which cortical neurons reached SNr via direct and indirect pathways.

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Diffusion MRI data, sulcal anatomy, and tractography for eight species from the Primate Brain Bank

Brain Structure and Function ◽

10.1007/s00429-021-02268-x ◽

2021 ◽

Author(s):

Katherine L. Bryant ◽

Dirk Jan Ardesch ◽

Lea Roumazeilles ◽

Lianne H. Scholtens ◽

Alexandre A. Khrapitchev ◽

...

Keyword(s):

Diffusion Mri ◽

Large Scale ◽

Structural Mri ◽

Relative Volume ◽

Primate Species ◽

Brain Bank ◽

Cingulum Bundle ◽

Primate Brain ◽

Multiple Levels ◽

Comparative Neuroscience

AbstractLarge-scale comparative neuroscience requires data from many species and, ideally, at multiple levels of description. Here, we contribute to this endeavor by presenting diffusion and structural MRI data from eight primate species that have not or rarely been described in the literature. The selected samples from the Primate Brain Bank cover a prosimian, New and Old World monkeys, and a great ape. We present preliminary labelling of the cortical sulci and tractography of the optic radiation, dorsal part of the cingulum bundle, and dorsal parietal–frontal and ventral temporal-frontal longitudinal white matter tracts. Both dorsal and ventral association fiber systems could be observed in all samples, with the dorsal tracts occupying much less relative volume in the prosimian than in other species. We discuss the results in the context of known primate specializations and present hypotheses for further research. All data and results presented here are available online as a resource for the scientific community.

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The Role of Primate Prefrontal Cortex in Bias and Shift Between Visual Dimensions

Cerebral Cortex ◽

10.1093/cercor/bhz072 ◽

2019 ◽

Vol 30 (1) ◽

pp. 85-99 ◽

Cited By ~ 5

Author(s):

Farshad A Mansouri ◽

Mark J Buckley ◽

Daniel J Fehring ◽

Keiji Tanaka

Keyword(s):

Prefrontal Cortex ◽

Anterior Cingulate ◽

Top Down ◽

Attentional Processes ◽

Prefrontal Cortical ◽

Frontopolar Cortex ◽

Dorsolateral Prefrontal ◽

Cortical Regions ◽

Visual Cortical ◽

Bilateral Lesions

Abstract Imaging and neural activity recording studies have shown activation in the primate prefrontal cortex when shifting attention between visual dimensions is necessary to achieve goals. A fundamental unanswered question is whether representations of these dimensions emerge from top-down attentional processes mediated by prefrontal regions or from bottom-up processes within visual cortical regions. We hypothesized a causative link between prefrontal cortical regions and dimension-based behavior. In large cohorts of humans and macaque monkeys, performing the same attention shifting task, we found that both species successfully shifted between visual dimensions, but both species also showed a significant behavioral advantage/bias to a particular dimension; however, these biases were in opposite directions in humans (bias to color) versus monkeys (bias to shape). Monkeys’ bias remained after selective bilateral lesions within the anterior cingulate cortex (ACC), frontopolar cortex, dorsolateral prefrontal cortex (DLPFC), orbitofrontal cortex (OFC), or superior, lateral prefrontal cortex. However, lesions within certain regions (ACC, DLPFC, or OFC) impaired monkeys’ ability to shift between these dimensions. We conclude that goal-directed processing of a particular dimension for the executive control of behavior depends on the integrity of prefrontal cortex; however, representation of competing dimensions and bias toward them does not depend on top-down prefrontal-mediated processes.

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