Research Article

Flexible recruitment of memory-based choice representations by the human medial frontal cortex

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Science  26 Jun 2020:
Vol. 368, Issue 6498, eaba3313
DOI: 10.1126/science.aba3313

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The adaptive human frontal cortex

Flexibly switching between different tasks is a fundamental human cognitive ability that allows us to make selective use of only the information needed for a given decision. Minxha et al. used single-neuron recordings from patients to understand how the human brain retrieves memories on demand when needed for making a decision and how retrieved memories are dynamically routed in the brain from the temporal to the frontal lobe. When memory was not needed, only medial frontal cortex neural activity was correlated with the task. However, when outcome choices required memory retrieval, frontal cortex neurons were phase-locked to field potentials recorded in the medial temporal lobe. Therefore, depending on demands of the task, neurons in different regions can flexibly engage and disengage their activity patterns.

Science, this issue p. eaba3313

Structured Abstract

INTRODUCTION

Decision-making in complex environments relies on flexibly combining stimulus representations with context, goals, and memories. A central component of cognitive flexibility is to selectively retrieve information from memory and utilize the retrieved information to make decisions. The medial frontal cortex (MFC) plays a critical role in this process by representing task sets, context, and outcomes. During decision-making, the MFC is thought to selectively engage memory retrieval by representing memory-based choices and mediating interactions between the frontal lobes and the hippocampus and amygdala (HA) through phase-locking of MFC activity to oscillations in the HA. It remains unknown what features of decisions and context are represented in the human MFC and what functional interactions between the MFC and HA mediate dynamic memory retrieval during a task.

RATIONALE

We recorded single neurons and local field potentials in the human MFC and HA in patients implanted with depth electrodes. Subjects switched between two tasks: recognition memory and categorization. To identify signatures of task demands, we compared the strength of encoding of stimulus familiarity, category, and choices between tasks and tested whether decoders trained in one task generalized to the other task. Such cross-task generalizability would indicate abstract representations of the underlying variables. We hypothesized that this approach would reveal neural signatures of the representations and functional interactions that permit memory-based decisions.

RESULTS

We recorded from 1430 single neurons in the HA and MFC [dorsal anterior cingulate cortex (dACC) and the pre-supplementary motor area (pre-SMA)] across 13 patients. Subjects made “yes” or “no” decisions using button presses or saccades (eye movements) to indicate whether an image was novel or familiar, or whether an image belonged to a given visual category. Instructions were given before each block of trials, explaining the task and response modality to use (i.e., task set). Examining the underlying neural representations at the single-neuron and population levels revealed the following: (i) Cells in the MFC represented task set during baseline periods. These contextual signals emerged rapidly after a task switch and generalized across all response and task-type combinations in the MFC but not the HA. (ii) The strength and geometry of representations of familiarity were task-insensitive in the HA but not in the MFC. The responses of these memory-selective cells were a reflection of memory strength rather than decisions about the memory. (iii) The visual category of stimuli was represented more strongly during the memory task in both the MFC and HA. This encoding of category generalized across tasks fully in the HA but not the MFC. (iv) Choices in both tasks were most strongly represented by cells in the MFC. This choice representation differed in its population-level geometry between the two tasks but was insensitive to response modality (button press or saccade). One subset of MFC cells signaled only memory-based choices, and these cells signaled decisions about the memory. (v) MFC cells phase-locked their activity to theta-frequency band oscillation in the HA preferentially in the memory task, with memory-choice cells also phase-locking in the gamma-frequency band. The strength of this interareal phase-locking in both frequency bands of the MFC cells that signaled memory-based choices was predictive of behavior.

CONCLUSION

We leveraged the opportunity to record from single neurons in humans to identify representations of choices, task sets, stimulus category, and familiarity in the human MFC and HA. We found that neuronal populations within the MFC formed two separate decision axes: one for memory-based decisions and another for categorization-based decisions. MFC-HA theta-frequency functional connectivity was selectively enhanced during memory retrieval. This work reveals a neuronal mechanism in the human brain whereby oscillation-mediated coordination of activity between distant brain regions and accompanying changes in strength of representation and/or geometry implements task-dependent retrieval of memory.

Flexible representations of choices in the human frontal lobe.

(A) Recording locations. LFP, local field potential. (B) Population response of all recorded neurons (left) and example of a cell signaling memory-based choices (right). (C and D) Representational geometry analysis reveals that different subspaces are used by the two tasks, establishing a memory-specific decision axis. (E) Theta- and gamma-band coherence of MFC choice cells with HA LFPs increased during the memory task.

Abstract

Decision-making in complex environments relies on flexibly using prior experience. This process depends on the medial frontal cortex (MFC) and the medial temporal lobe, but it remains unknown how these structures implement selective memory retrieval. We recorded single neurons in the MFC, amygdala, and hippocampus while human subjects switched between making recognition memory–based and categorization-based decisions. The MFC rapidly implemented changing task demands by using different subspaces of neural activity and by representing the currently relevant task goal. Choices requiring memory retrieval selectively engaged phase-locking of MFC neurons to amygdala and hippocampus field potentials, thereby enabling the routing of memories. These findings reveal a mechanism for flexibly and selectively engaging memory retrieval and show that memory-based choices are preferentially represented in the frontal cortex when required.

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