Oxford Centre for Computational Neuroscience

Professor Edmund T. Rolls

Discoveries on Human Cortical Connectivity

Cerebral Cortex

The Noisy Brain

Emotion Explained

Memory, Attention, and Decision-Making


Neural Networks and Brain Function

Overview: Rolls has developed investigations into the effective connectivity of the human cerebral cortex complemented by functional connectivity and diffusion tractography, utilising 360 cortical regions defined in the Human Connectome Project Multimodal Parcellation (HCP-MMP) atlas (Glasser et al 2016 Nature 536: 171-178; 645), data from the Human Connectome Project at 7T, and an effective connectivity algorithm developed by Gustavo Deco (647, 656). These investigations provide great insight into cortical processing streams as described next, and are making key contributions to understanding what computations are performed by each brain region given its connectivity (B16).

Cortical visual streams (656, B16)

A Ventrolateral Visual ‘What’ Stream for object and face recognition projects hierarchically to the inferior temporal visual cortex which projects to the orbitofrontal cortex for reward value and emotion, and to the hippocampal memory system.

A Ventromedial Visual Stream has connectivity via the ventromedial visual areas to the parahippocampal scene (or place) area that builds scenes utilising overlapping ventral visual stream features, and thereby provides a ventral stream 'where' input to the human hippocampus (656). The concept and connectivity are new and are leading towards a better understanding of hippocampal function in memory and navigation in primates including humans (662).

A Dorsal Visual Stream connects via V2 and V3A to MT+ Complex regions (including MT and MST), which connect to intraparietal regions (including LIP, VIP and MIP) involved in visual motion and actions in space. It performs coordinate transforms for idiothetic update of Ventromedial Stream scene representations (656, 662, 655, 612).

Connectivity has been discovered from inferior parietal PGp  (which receives from parietal area 7 regions) to the hippocampus which is implicated in the self-motion (idiothetic) update of parahippocampal and hippocampal spatial view cells using eye position and head direction information (656, 655, 612, 662).

It has been discovered that an Inferior bank of the STS (superior temporal sulcus) cortex Semantic Stream receives from the Ventrolateral Visual Stream, from visual inferior parietal PGi, and from the ventromedial-prefrontal cortex reward system and connects to language systems (656, 654).

It has been discovered that a Superior bank of the STS cortex Semantic Stream receives visual inputs from the Inferior STS Visual Stream, inferior parietal PGi, and STV, and auditory inputs from A5, is activated by face expression, motion and vocalization, and is important in social behaviour, and connects to language systems (656, 654).

Posterior parietal cortex (655, B16)

Intraparietal areas LIP, VIP, MIP, and AIP have connectivity from early cortical visual regions, and to visuomotor regions such as the frontal eye fields, consistent with functions in eye saccades and tracking. Five superior parietal area 7 regions receive from similar areas and from the intraparietal areas, but also receive somatosensory inputs and connect with premotor areas including area 6, consistent with functions in performing actions to reach for, grasp, and manipulate objects.

In the anterior inferior parietal cortex, PFop, PFt and PFcm are mainly somatosensory, and PF in addition receives visuo-motor and visual object information, and is implicated in multimodal shape and body image representations.

In the posterior inferior parietal cortex, PFm and PGs combine visuo-motor, visual object, and reward input and connect with the hippocampal system. PGi in addition provides a route to motion-related superior temporal sulcus regions involved in social interactions. PGp has connectivity with intraparietal regions involved in coordinate transforms and may be involved in idiothetic update of hippocampal and parahippocampal cortex visual scene representations (655, 662).

Orbitofrontal cortex, vmPFC, anterior cingulate cortex, and amygdala (649, 665, 657, B16)

The orbitofrontal cortex has effective connectivity from gustatory, olfactory, and temporal visual, auditory and pole cortical areas. The orbitofrontal cortex has connectivity to the pregenual anterior and posterior cingulate cortex and hippocampal system, and provides for rewards to be used in memory and navigation to goals.

The orbitofrontal and pregenual anterior cortex have connectivity to the supracallosal anterior cingulate cortex which projects to midcingulate and other premotor cortical areas, and provide for action-outcome learning including limb withdrawal or flight or fight to aversive and non-reward stimuli.

The lateral orbitofrontal cortex has outputs to language systems in the inferior frontal gyrus and provides a route for declarative reports about emotional states.

In contrast, the amygdala has relatively little connectivity back to the neocortex in humans, and so may be less involved in consciously experienced emotion than in behavioural and autonomic responses to punishing and rewarding stimuli (665).

The medial orbitofrontal cortex connects to the nucleus basalis of Meynert and the pregenual anterior cingulate to the septum, and damage to these cortical regions may contribute to memory impairments by disrupting cholinergic influences on the neocortex and hippocampus normally involved in memory consolidation (649, 657).

Hippocampal systems for memory and navigation (657, 656, 655, 649, 647, 644, 635, 662, B16)

The connectivity from the human orbitofrontal cortex, vmPFC and anterior cingulate cortex to the hippocampal system shows how reward value and emotion can reach the hippocampal memory system to become incorporated into episodic memory (649, 657, 635, 644). This also shows how these cortical regions have connectivity with the septum and basal forebrain cholinergic systems, providing a mechanism that may contribute to the memory impairments produced by vmPFC damage in humans (649, 657). These discoveries lead to a new approach to memory consolidation that incorporates the roles of reward systems in memory consolidation (657).

The identification in humans using effective connectivity of a ventromedial visual stream via the ventromedial visual areas to the parahippocampal scene (or place) area which builds scenes by overlapping ventral visual stream features and thereby provides a ventral stream 'where' input to the hippocampus (656). This concept and discovery is beyond anything known in rodents, and relates to spatial view cells (662, B16).

The identification in humans of a pathway from inferior parietal PGp  which receives from parietal area 7 regions to the hippocampus which is implicated in the self-motion (idiothetic) update of parahippocampal and hippocampal spatial view cells using eye position and head direction information (656, 655, 612). This is likely to be involved in navigation and memory in the dark and when the view details are obscured (662).

The identification in humans of connectivity from the Lateral Ventral Visual Stream to the lateral temporal lobe for object and face representations via parahippocampal TF to the hippocampus to provide 'what' information for the human hippocampal memory system (656, 662).

The identification in humans of the connectivity of a transitional cortical area, the posterior cingulate cortex (not present in rodents) between the neocortex and the hippocampus (661). A posterior part of the posterior cingulate regions has connectivity with 'what' systems and the hippocampus, and an anterior part with 'where' systems, and both provide routes to and from the hippocampal memory system (661, B16).

Cortical systems for language (654, B16)

A 'what and reward' semantic system has been identified involving cortex in the ventral banks of the superior temporal sulcus, the temporal pole, inferior parietal PGi, and orbitofrontal cortex; and a visual face and object motion and auditory semantic system in the dorsal bank of the superior temporal temporal sulcus cortex especially implicated in social semantics (654). Both semantic systems have effective connectivity to Broca's area 44 and 45, which in humans has links to other nearby inferior frontal cortex regions that are proposed to provide attractor networks for syntactic computations (654, 537).

Auditory cortical pathways in humans (666, B16)

It has been possible to follow the connectivity of the human auditory system from core auditory cortex through belt and parabelt to A4, A5 and thereby to language areas of the human cerebral cortex (666).

Somatosensory cortical pathways in humans (660, B16)

It has been possible to follow the connectivity of the human somatosensory system from areas 3, 2 and 1 via the opercular and frontal opercular cortical regions to the insula, and thereby to the inferior parietal somatosensory regions PFop and PF, and to show that PF also receives visual inputs making it not only the top of the human somatosensory hierarchy, but also a multimodal region for the representation of felt and grasped objects (660).

Prefrontal cortical regions for working memory and executive function in humans (660, B16)

It has been possible to show in humans that inferior prefrontal regions have connectivity with the inferior temporal visual cortex and orbitofrontal cortex, are implicated in working memory for “what” processing streams, and provide connectivity to language systems, including 44, 45, 47l, TPOJ1, and the superior temporal visual area, for which it is proposed that they also provide attractor networks (660, 654). The dorsolateral prefrontal cortex regions that include area 46 have connectivity with parietal area 7 and somatosensory inferior parietal regions and are implicated in working memory for actions and planning. The dorsal prefrontal regions, including 8Ad and 8Av, have connectivity with visual regions of the inferior parietal cortex, including PGs and PGi, and are implicated in visual and auditory top-down attention ( 660).