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Perirhinal circuits for memory processing

Abstract

The perirhinal cortex (PRC) serves as the gateway to the hippocampus for episodic memory formation and plays a part in retrieval through its backward connectivity to various neocortical areas. First, I present the evidence suggesting that PRC neurons encode both experientially acquired object features and their associative relations. Recent studies have revealed circuit mechanisms in the PRC for the retrieval of cue-associated information, and have demonstrated that, in monkeys, PRC neuron-encoded information can be behaviourally read out. These studies, among others, support the theory that the PRC converts visual representations of an object into those of its associated features and initiates backward-propagating, interareal signalling for retrieval of nested associations of object features that, combined, extensionally represent the object meaning. I propose that the PRC works as the ventromedial hub of a ‘two-hub model’ at an apex of the hierarchy of a distributed memory network and integrates signals encoded in other downstream cortical areas that support diverse aspects of knowledge about an object.

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Fig. 1: Location of the perirhinal cortex and its connectivity.
Fig. 2: What emerges in the perirhinal cortex along the ventral visual pathway.
Fig. 3: Linking cue stimuli and target stimuli in the perirhinal cortex.
Fig. 4: Backward output from the perirhinal cortex to lower-order cortical areas for memory retrieval.

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Acknowledgements

This research was supported in part by MEXT and the Japan Society for the Promotion of Science KAKENHI grants 17H06161 and 24220008.

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Glossary

Structural encoding

An early-stage encoding process in cognition that emphasizes the physical structure of the stimulus. Automatically proceeds even in a shallow encoding condition. Particularly well analysed and theorized in face recognition.

Ventral visual pathway

A functional stream involved in visual analyses of objects in the primate brain. Also called the ‘what pathway’. Anatomically, visual input from area V1 is projected to areas TEO and TE via areas V2 and V4.

Nested associations

In a semantic network model, nodes and arcs are hierarchically organized to form associative knowledge representations. Spreading activation along the arcs retrieves the nested associative representation.

Hub-and-spoke model

A hypothesis of the structure and neural basis of semantic memory. Many cortical regions represent an aspect of conceptual knowledge that is modality specific. The links between each modality-specific region and a supramodal hub region are called ‘spokes’.

Recency neurons

A group of neurons in the anterior temporal cortex of monkeys that encode information whether or not a stimulus has been seen recently, regardless of whether it is relatively familiar or not.

Repetition priming

Improvements in a behavioural response when stimuli are repeatedly presented. The improvements can be measured in terms of accuracy or reaction time.

Agranular cortex

A cytoarchitecturally defined term denoting the type of heterotypic cortex that is distinguished by the lack of granule cells. An area of cortex that is only slightly granulated is termed ‘dysgranular’.

Lexicosemantic association area

Brain areas that are devoted to the analysis and understanding of the meaning of the lexical units (words and subwords) and of the relations between the word meaning and structure of the language.

Current sink

From extracellular electric potentials recorded at multiple sites, current sources and sinks generating the measured potentials are estimated. Typically, the current sinks indicate the locations of synapses generating excitatory postsynaptic potentials.

Receptive fields

Portions of sensory space that can elicit neuronal responses when stimulated. In vision, the sensory space can be defined in multiple dimensions, such as space, time and tuning properties.

Matching-to-sample test

A form of conditional discrimination. Short-term memory or working memory has been studied with this test. A participant is asked to first encode a stimulus and later to make a forced-choice response among options where one option corresponds to that stimulus.

Cross-modal matching test

In the matching-to-sample test, the correct response option typically corresponds directly in some way to the stimulus (for example, the response option and stimulus are the same colour). However, the test can require a symbolic match or a matching based on the identity of the object. For example, participants are asked to cross-modally match visual and auditory displays on the basis of the identity of the speaker or sound source.

Face-patch network

Specialized brain areas that primates have evolved to extract multidimensional facial information are called ‘face patches’. They are tightly and specifically interconnected to form a face-processing system.

Repetition suppression

The reduction in neural activity when stimuli are repeated. It can occur across a range of repetition time lags, even when multiple interleaving stimuli are presented with the repeated stimulus.

Stimulus–reward associations

An ability to assign value to stimuli, or to link objects with the affective qualities of reward, on the basis of reinforcement history. Amygdala plays a key role in this association.

Trigger features

A particular feature of a stimulant which causes a reaction within a particular neuron. In the primate temporal cortex, trigger features become complex, including hands or faces.

Cued-recall task

A procedure for testing memory in which a participant is presented with cues, such as words or objects, to aid recall of previously experienced stimuli. Cued recall also occurs in everyday life.

Memory traces

A transient or long-term change in the brain that provides a physical basis for the persistence of memory. Also called ‘memory engram’.

Retrospection

A reconsideration of something that happened in the past, typically of something involving one’s own experiences.

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Miyashita, Y. Perirhinal circuits for memory processing. Nat Rev Neurosci 20, 577–592 (2019). https://doi.org/10.1038/s41583-019-0213-6

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