The human posterior parietal cortex: effective connectome, and its relation to function.

The effective connectivity between 21 regions in the human posterior parietal cortex, and 360 cortical regions was measured in 171 Human Connectome Project (HCP) participants using the HCP atlas, and complemented with functional connectivity and diffusion tractography. 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 visual scene representations.

Multiple cortical visual streams in humans.

The effective connectivity between 55 visual cortical regions and 360 cortical regions was measured in 171 HCP participants using the HCP-MMP atlas, and complemented with functional connectivity and diffusion tractography. 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 "Where" Stream for scene representations connects to the parahippocampal gyrus and hippocampus. An Inferior STS (superior temporal sulcus) cortex Semantic Stream receives from the Ventrolateral Visual Stream, from visual inferior parietal PGi, and from the ventromedial-prefrontal reward system and connects to language systems. 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. A Superior STS cortex Semantic Stream receives visual inputs from the Inferior STS Visual Stream, 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.

Hippocampal spatial view cells for memory and navigation, and their underlying connectivity in humans.

Hippocampal and parahippocampal gyrus spatial view neurons in primates respond to the spatial location being looked at. The representation is allocentric, in that the responses are to locations "out there" in the world, and are relatively invariant with respect to retinal position, eye position, head direction, and the place where the individual is located. The underlying connectivity in humans is from ventromedial visual cortical regions to the parahippocampal scene area, leading to the theory that spatial view cells are formed by combinations of overlapping feature inputs self-organized based on their closeness in space. Thus, although spatial view cells represent "where" for episodic memory and navigation, they are formed by ventral visual stream feature inputs in the parahippocampal gyrus in what is the parahippocampal scene area. A second "where" driver of spatial view cells are parietal inputs, which it is proposed provide the idiothetic update for spatial view cells, used for memory recall and navigation when the spatial view details are obscured. Inferior temporal object "what" inputs and orbitofrontal cortex reward inputs connect to the human hippocampal system, and in macaques can be associated in the hippocampus with spatial view cell "where" representations to implement episodic memory. Hippocampal spatial view cells also provide a basis for navigation to a series of viewed landmarks, with the orbitofrontal cortex reward inputs to the hippocampus providing the goals for navigation, which can then be implemented by hippocampal connectivity in humans to parietal cortex regions involved in visuomotor actions in space. The presence of foveate vision and the highly developed temporal lobe for object and scene processing in primates including humans provide a basis for hippocampal spatial view cells to be key to understanding episodic memory in the primate and human hippocampus, and the roles of this system in primate including human navigation.

Hippocampal spatial view cells, place cells, and concept cells: View representations.

A commentary is provided on issues raised in the Special Issue of Hippocampus (2023) on hippocampal system view representations. First, the evidence for hippocampal and parahippocampal spatial view cells in primates including humans shows that the allocentric representations provided by at least some of these cells are very useful for human memory in that where objects and rewards are seen in the world "out there" is a key component of episodic memory and navigation. Spatial view cell representations provide for memory and navigation to be independent of the place where the individual is currently located and of the egocentric coordinates of the viewed location and the facing direction of the individual. Second, memory and navigation in humans are normally related to the visual cues encoded by spatial view cells that define a location "out there" such as a building, hill, and so forth, not to an unmarked place without local cues and identified only by distant environmental/room cues. Third, "mixed" representations, for example of particular combinations of spatial view and place, can arise if the training has been for only some combinations of place and view, for that is what can then be learned by the hippocampus. Fourth, rodents, with their much less good visual acuity (~1 cycle/° in rats, compared with ~60 cycles/° for the human fovea), and rodents' very wide viewing angle for the world (~270°) might be expected, when using the same computational mechanisms as in primates, to use widely spaced environmental cues to define a place where the rodent is located, supported by inputs about place using local olfactory and tactile cues. Fifth, it is shown how view-point dependent allocentric representations could form a view-point independent allocentric representation for memory and navigation. Sixth, concept cells in humans and primates with connectivity to the hippocampus are compared.

The human posterior cingulate, retrosplenial, and medial parietal cortex effective connectome, and implications for memory and navigation.

The human posterior cingulate, retrosplenial, and medial parietal cortex are involved in memory and navigation. The functional anatomy underlying these cognitive functions was investigated by measuring the effective connectivity of these Posterior Cingulate Division (PCD) regions in the Human Connectome Project-MMP1 atlas in 171 HCP participants, and complemented with functional connectivity and diffusion tractography. First, the postero-ventral parts of the PCD (31pd, 31pv, 7m, d23ab, and v23ab) have effective connectivity with the temporal pole, inferior temporal visual cortex, cortex in the superior temporal sulcus implicated in auditory and semantic processing, with the reward-related vmPFC and pregenual anterior cingulate cortex, with the inferior parietal cortex, and with the hippocampal system. This connectivity implicates it in hippocampal episodic memory, providing routes for "what," reward and semantic schema-related information to access the hippocampus. Second, the antero-dorsal parts of the PCD (especially 31a and 23d, PCV, and also RSC) have connectivity with early visual cortical areas including those that represent spatial scenes, with the superior parietal cortex, with the pregenual anterior cingulate cortex, and with the hippocampal system. This connectivity implicates it in the "where" component for hippocampal episodic memory and for spatial navigation. The dorsal-transitional-visual (DVT) and ProStriate regions where the retrosplenial scene area is located have connectivity from early visual cortical areas to the parahippocampal scene area, providing a ventromedial route for spatial scene information to reach the hippocampus. These connectivities provide important routes for "what," reward, and "where" scene-related information for human hippocampal episodic memory and navigation. The midcingulate cortex provides a route from the anterior dorsal parts of the PCD and the supracallosal part of the anterior cingulate cortex to premotor regions.

Neurons including hippocampal spatial view cells, and navigation in primates including humans.

A new theory is proposed of mechanisms of navigation in primates including humans in which spatial view cells found in the primate hippocampus and parahippocampal gyrus are used to guide the individual from landmark to landmark. The navigation involves approach to each landmark in turn (taxis), using spatial view cells to identify the next landmark in the sequence, and does not require a topological map. Two other cell types found in primates, whole body motion cells, and head direction cells, can be utilized in the spatial view cell navigational mechanism, but are not essential. If the landmarks become obscured, then the spatial view representations can be updated by self-motion (idiothetic) path integration using spatial coordinate transform mechanisms in the primate dorsal visual system to transform from egocentric to allocentric spatial view coordinates. A continuous attractor network or time cells or working memory is used in this approach to navigation to encode and recall the spatial view sequences involved. I also propose how navigation can be performed using a further type of neuron found in primates, allocentric-bearing-to-a-landmark neurons, in which changes of direction are made when a landmark reaches a particular allocentric bearing. This is useful if a landmark cannot be approached. The theories are made explicit in models of navigation, which are then illustrated by computer simulations. These types of navigation are contrasted with triangulation, which requires a topological map. It is proposed that the first strategy utilizing spatial view cells is used frequently in humans, and is relatively simple because primates have spatial view neurons that respond allocentrically to locations in spatial scenes. An advantage of this approach to navigation is that hippocampal spatial view neurons are also useful for episodic memory, and for imagery.

Spatial coordinate transforms linking the allocentric hippocampal and egocentric parietal primate brain systems for memory, action in space, and navigation.

A theory and model of spatial coordinate transforms in the dorsal visual system through the parietal cortex that enable an interface via posterior cingulate and related retrosplenial cortex to allocentric spatial representations in the primate hippocampus is described. First, a new approach to coordinate transform learning in the brain is proposed, in which the traditional gain modulation is complemented by temporal trace rule competitive network learning. It is shown in a computational model that the new approach works much more precisely than gain modulation alone, by enabling neurons to represent the different combinations of signal and gain modulator more accurately. This understanding may have application to many brain areas where coordinate transforms are learned. Second, a set of coordinate transforms is proposed for the dorsal visual system/parietal areas that enables a representation to be formed in allocentric spatial view coordinates. The input stimulus is merely a stimulus at a given position in retinal space, and the gain modulation signals needed are eye position, head direction, and place, all of which are present in the primate brain. Neurons that encode the bearing to a landmark are involved in the coordinate transforms. Part of the importance here is that the coordinates of the allocentric view produced in this model are the same as those of spatial view cells that respond to allocentric view recorded in the primate hippocampus and parahippocampal cortex. The result is that information from the dorsal visual system can be used to update the spatial input to the hippocampus in the appropriate allocentric coordinate frame, including providing for idiothetic update to allow for self-motion. It is further shown how hippocampal spatial view cells could be useful for the transform from hippocampal allocentric coordinates to egocentric coordinates useful for actions in space and for navigation.

A scientific theory of Ars Memoriae: Spatial view cells in a continuous attractor network with linked items.

The art of memory (ars memoriae) used since classical times includes using a well-known scene to associate each view or part of the scene with a different item in a speech. This memory technique is also known as the "method of loci." The new theory is proposed that this type of memory is implemented in the CA3 region of the hippocampus where there are spatial view cells in primates that allow a particular view to be associated with a particular object in an event or episodic memory. Given that the CA3 cells with their extensive recurrent collateral system connecting different CA3 cells, and associative synaptic modifiability, form an autoassociation or attractor network, the spatial view cells with their approximately Gaussian view fields become linked in a continuous attractor network. As the view space is traversed continuously (e.g., by self-motion or imagined self-motion across the scene), the views are therefore successively recalled in the correct order, with no view missing, and with low interference between the items to be recalled. Given that each spatial view has been associated with a different discrete item, the items are recalled in the correct order, with none missing. This is the first neuroscience theory of ars memoriae. The theory provides a foundation for understanding how a key feature of ars memoriae, the ability to use a spatial scene to encode a sequence of items to be remembered, is implemented. © 2017 Wiley Periodicals, Inc.

The hippocampus, ventromedial prefrontal cortex, and episodic and semantic memory.

The human ventromedial prefrontal cortex (vmPFC)/anterior cingulate cortex is implicated in reward and emotion, but also in memory. It is shown how the human orbitofrontal cortex connecting with the vmPFC and anterior cingulate cortex provide a route to the hippocampus for reward and emotional value to be incorporated into episodic memory, enabling memory of where a reward was seen. It is proposed that this value component results in primarily episodic memories with some value component to be repeatedly recalled from the hippocampus so that they are more likely to become incorporated into neocortical semantic and autobiographical memories. The same orbitofrontal and anterior cingulate regions also connect in humans to the septal and basal forebrain cholinergic nuclei, thereby helping to consolidate memory, and helping to account for why damage to the vMPFC impairs memory. The human hippocampus and vmPFC thus contribute in complementary ways to forming episodic and semantic memories.

Learning Invariant Object and Spatial View Representations in the Brain Using Slow Unsupervised Learning.

First, neurophysiological evidence for the learning of invariant representations in the inferior temporal visual cortex is described. This includes object and face representations with invariance for position, size, lighting, view and morphological transforms in the temporal lobe visual cortex; global object motion in the cortex in the superior temporal sulcus; and spatial view representations in the hippocampus that are invariant with respect to eye position, head direction, and place. Second, computational mechanisms that enable the brain to learn these invariant representations are proposed. For the ventral visual system, one key adaptation is the use of information available in the statistics of the environment in slow unsupervised learning to learn transform-invariant representations of objects. This contrasts with deep supervised learning in artificial neural networks, which uses training with thousands of exemplars forced into different categories by neuronal teachers. Similar slow learning principles apply to the learning of global object motion in the dorsal visual system leading to the cortex in the superior temporal sulcus. The learning rule that has been explored in VisNet is an associative rule with a short-term memory trace. The feed-forward architecture has four stages, with convergence from stage to stage. This type of slow learning is implemented in the brain in hierarchically organized competitive neuronal networks with convergence from stage to stage, with only 4-5 stages in the hierarchy. Slow learning is also shown to help the learning of coordinate transforms using gain modulation in the dorsal visual system extending into the parietal cortex and retrosplenial cortex. Representations are learned that are in allocentric spatial view coordinates of locations in the world and that are independent of eye position, head direction, and the place where the individual is located. This enables hippocampal spatial view cells to use idiothetic, self-motion, signals for navigation when the view details are obscured for short periods.

Spatial representations in the primate hippocampus, and their functions in memory and navigation.

Hippocampal spatial view neurons in primates respond to the place where a monkey is looking, with some modulation by place. In contrast, hippocampal neurons in rodents respond mainly to the place where the animal is located. We relate this difference to the development of a fovea in primates, and the highly developed primate visual system which enables identification of what is at the fovea, and a system for moving the eyes to view different parts of the environment. We show that the spatial view representation in primates is allocentric, and provide new animations using recorded neuronal activity to illustrate this. We also show that this spatial representation becomes engaged in tasks in which the location 'out there' in a scene of objects and rewards must be remembered. We show that this representation of space being viewed provides a framework for the encoding of episodic memory and the recall of these memories in primates including humans, with hippocampal neurons responding for example in a one-trial object / place recall task. These functions of the primate hippocampus in scene-related memory, provide a way for the primate hippocampus to contribute to actions in space and navigation. We consider in a formal model the mechanisms by which these different spatial representations may be formed given the presence of the primate fovea, and how these mechanisms may contribute to the representations found during navigation in a virtual environment.

A quantitative theory of the functions of the hippocampal CA3 network in memory.

A quantitative computational theory of the operation of the hippocampal CA3 system as an autoassociation or attractor network used in episodic memory system is described. In this theory, the CA3 system operates as a single attractor or autoassociation network to enable rapid, one-trial, associations between any spatial location (place in rodents, or spatial view in primates) and an object or reward, and to provide for completion of the whole memory during recall from any part. The theory is extended to associations between time and object or reward to implement temporal order memory, also important in episodic memory. The dentate gyrus (DG) performs pattern separation by competitive learning to produce sparse representations suitable for setting up new representations in CA3 during learning, producing for example neurons with place-like fields from entorhinal cortex grid cells. The dentate granule cells produce by the very small number of mossy fiber (MF) connections to CA3 a randomizing pattern separation effect important during learning but not recall that separates out the patterns represented by CA3 firing to be very different from each other, which is optimal for an unstructured episodic memory system in which each memory must be kept distinct from other memories. The direct perforant path (pp) input to CA3 is quantitatively appropriate to provide the cue for recall in CA3, but not for learning. Tests of the theory including hippocampal subregion analyses and hippocampal NMDA receptor knockouts are described, and support the theory.