Oxford Centre for Computational Neuroscience

Professor Edmund T. Rolls

Discoveries on the Neuroscience of Memory, Spatial Function, and Navigation

Cerebral Cortex

The Noisy Brain

Memory, Attention, and Decision-Making

Neural Networks and Brain Function

Overview: Rolls and colleagues discovered spatial view neurons, object-and-spatial view neurons, reward-and-spatial view neurons, and whole body motion neurons (termed 'speed cells' in rodents) in the hippocampus, and head direction cells in the presubiculum, of primates. These neurons provide a foundation for understanding how the primate including human hippocampal system operates in episodic memory, and navigation to landmarks. The neurophysiological discoveries are complemented by a theory of how neuronal networks in the hippocampal system operate using pattern separation and pattern completion, and what remains the only quantitative theory of how information is recalled from the hippocampus to the neocortex. Developments in understanding the effective connectivity of the hippocampal system in humans lead to a new approach to episodic memory in which a key component of episodic memory is reward / emotional value from the orbitofrontal cortex (657, 649, 647) which is combined in the hippocampus with 'what' information about objects and faces from the inferior temporal cortex (656) and 'where' information about scenes from the ventromedial visual stream to the parahippocampal scene area (656). This in turn leads to a new approach to memory consolidation in which the reward component of episodic memory influences memory consolidation in the neocortex, acting in part by the orbitofrontal cortex input to the basal forebrain cholinergic neurons (657, 665).  Key summary descriptions are in 657, 665, 633, B16, 584, 594, 539, 550 and 186.

The discovery of hippocampal and parahippocampal spatial view neurons that provide an allocentric representation of spatial locations being viewed, and that are updated by self-motion (129, 152, 202, 237, 244, 247, 256, 267, 594, B16, 633, 662, 672).


The discovery of hippocampal spatial view neurons that combine information about spatial view and the objects (130, 131, 380) or rewards (387), and are involved in recall (399), providing a basis for implementing episodic memory (657, 662, 539, B12, 594, 662, 672, B16).

A theory for how hippocampal spatial view cells are involved in memory and navigation (584, 594, 539, B12, B16, 633, 662, 672) .


Hippocampal neurons in primates that respond to a combination of spatial view and place, or to place (202).


The discovery of whole-body motion neurons in the hippocampus (184), more recently termed 'speed cells'. These are relevant to hippocampal spatial representation update by self-motion, i.e. idiothetic update (633).


Hippocampal neurons that respond to a combination of spatial view and whole body motion (184, 202).


Head direction cells in the primate presubiculum (271).


The discovery of a representation of long-term familiarity memory in the perirhinal cortex, which may contribute to ownership (343, 388).

A theory and model of hippocampal operation and episodic memory, including pattern separation and pattern completion (111, 125, 136, 163, 186, 200, 205, 258, 266, 268, 300, 306, 307, 309, 345, 370, 403, 411, 415, 433, 453, 479, 504, 507, 521, 527, 529, 531, 539, 545, 550, 571, 584, 643, 672, B12, B16).

Extensive cortical connectivity of the human hippocampal memory system shown by diffusion tractography (635), functional connectivity (644), and effective connectivity (647, B16).

A recent discovery is of the effective connectivity of the  human orbitofrontal cortex, vmPFC and anterior cingulate cortex, which shows how reward value and emotion can reach the hippocampal memory system to become incorporated in episodic memory (649, 657, B16). 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).

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 'where' input to the hippocampus (656, 662, B16).

The identification in humans of a pathway from inferior parietal PGp  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, B16).

A theory and model of the generation of time in the hippocampal memory system which can provide a 'when' component of episodic memory. Entorhinal cortex time ramping cells produce through a competitive network hippocampal time cells, providing neuronal mechanisms to encode the order of events (605). The theory shows how cells could be generated that show 'replay' and 'reverse replay' (605, B16).

A theory and model of coordinate transforms in the dorsal visual system using a combination of gain modulation and slow or trace rule competitive learning. The theory starts with retinal position inputs gain modulated by eye position to produce a head centred representation, followed by gain modulation by head direction, followed by gain modulation by place, to produce an allocentric representation in spatial view coordinates useful for the idiothetic update of hippocampal spatial view cells (612). This is important in the theory of navigation using spatial view cells when the view details are obscured (633, 662, B16).

A theory of navigation in humans and other primates that utilizes hippocampal spatial view cells to navigate from landmark to landmark (633, 662, B16). This is an alternative to navigation involving place cells, and does not require a spatial cognitive Euclidean map. Idiothetic update by head direction and whole body motion cells is part of the theory (633). Allocentric bearing to a landmark cells may also be involved in a related type of navigation (633).

A theory of how spatial view cells and hippocampal attractor networks are involved in the art of memory (the method of loci) (571, 595).

Hypertension and impaired memory: even moderate hypertension is associated with reduced hippocampal functional connectivity and impaired memory (625).

The storage capacity of autoassociation and pattern association networks with sparse representations and diluted connectivity (150, 154, 222, 228, 515, 545, 672, B12, B16).

The discovery that basal forebrain, probably cholinergic neurons, that project to the cortex, have responses to forebrain-decoded reward, aversive, and novel stimuli (144, 145, 146, 177, B7, B11). These are thought to play a role in keeping the cerebral cortex alert to potentially important stimuli, and reducing the adaptation of cortical neurons, and in facilitating memory consolidation (657, B12, B16). In humans the basal forebrain  and septal regions receive inputs from the medial orbitofrontal and anterior cingulate cortex (649, 657). Reduction in the performance of this system may contribute to some of the cognitive changes during aging (B8, B9, B12, 540).


Mechanisms involving synaptic facilitation that enable several items to be held simultaneously in short-term memory (523) and that may be useful in the syntax for language (537).


Information can be retrieved from biologically plausible attractor neuronal networks very rapidly (in less than 2 time constants of the synapses) (with A.Treves and colleagues) (222, 235, 294). This makes cortical computation with attractor networks possible (B8, B12, B16).

The effective connectivity of the human prefrontal cortex using the HCP-MMP human brain atlas has identified different systems involved in working memory (660). 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 STV. 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). The underlying computational mechanisms have been described (B16).