Ventrolateral Prefrontal Neuronal Activity Related to Active Controlled Memory Retrieval in Nonhuman Primates

Abstract

It is controversial whether monkeys, like human subjects, can recall, upon instruction, specific information about an event in memory. We therefore tested macaque monkeys on a task that was originally developed to study such active controlled memory retrieval in human subjects and we were able to demonstrate that monkeys, like human subjects, can retrieve, upon command, specific components of previously encoded events. Furthermore, following earlier functional neuroimaging work with human subjects showing the mid-ventrolateral prefrontal cortex to be involved in such active controlled retrieval, we recorded single-neuron activity within this region of the monkey brain while the monkeys performed the active retrieval task. Neuronal responses were related to the retrieval and the decision whether the retrieved information was the instructed one. These findings demonstrate, for the first time, an impressive capacity by macaque monkeys for controlled memory retrieval and, in addition, provide neurophysiological evidence about the role of the mid-ventrolateral prefrontal cortex in such controlled retrieval.

Ventrolateral and dorsomedial frontal cortex lesions impair mnemonic context retrieval

“…The present results provide the first cause-and-effect confirmation of the essential role of the VLPFC in active retrieval processing necessary to disambiguate items and their context in memory, which had previously received support from neuroimaging studies on normal human subjects [15,20 -23] and single neuron recording in monkeys [45]. Petrides [15,16] argued that the ventrolateral prefrontal cortical region (areas 45 and 47/12) may be a critical part of the prefrontal cortex for the active controlled retrieval of information in situations in which items of information exist in memory under multiple associations with one another and, therefore, top-down control processing is necessary to disambiguate the memory traces that are assumed to lie in the posterior association neocortex.…”

“…After an instruction to retrieve a specific aspect of a recently memorized complex stimulus (e.g. to retrieve its colour, but not its shape), a class of neurons in the VLPFC responds selectively to the isolation of the instructed aspect of the memorized stimulus (see [45] for details). Thus, there is evidence of neuronal processing isolating particular aspects of memorized experiences.…”

Selective memory retrieval of auditory what and auditory where involves the ventrolateral prefrontal cortex

“…Recordings in nonhuman primates in the ventrolateral prefrontal cortex have provided evidence at the neuronal level for this active retrieval process. It has been shown that a class of neurons exhibits differential instruction-related activity according to the type of retrieval that must be performed by the monkey, thus signaling the initiation or noninitiation of the retrieval of specific information (44). A second class of neurons increase their firing rate during the delay after the instruction cue and before the test phase and, importantly, their firing is not modulated in the control trials or during the precue interval when the encoded event is simply stored in memory (44).…”

“…It has been shown that a class of neurons exhibits differential instruction-related activity according to the type of retrieval that must be performed by the monkey, thus signaling the initiation or noninitiation of the retrieval of specific information (44). A second class of neurons increase their firing rate during the delay after the instruction cue and before the test phase and, importantly, their firing is not modulated in the control trials or during the precue interval when the encoded event is simply stored in memory (44). Thus, the firing of these neurons is not related to encoding, maintenance, or simple recognition of an event in memory but rather to the active retrieval of specific features.…”

“…Thus, the firing of these neurons is not related to encoding, maintenance, or simple recognition of an event in memory but rather to the active retrieval of specific features. We conceptualize active retrieval as a top-down modulation of information within specific posterior cortical areas, that is, a type of attentional orienting toward a specific feature within a memory representation that leads to enhancement of the relevant feature and inhibition of the irrelevant features, resulting in successful retrieval of the required specific information (7,44). Importantly, there is evidence from studies of patients that the prefrontal cortex has a modulatory control role in activity in posterior auditory areas (45,46).…”