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

2019 ◽  
Author(s):  
Juri Minxha ◽  
Ralph Adolphs ◽  
Stefano Fusi ◽  
Adam N. Mamelak ◽  
Ueli Rutishauser

SummaryDecisions in complex environments rely on flexibly utilizing past experience as required by context and instructions1. This process depends on the medial frontal cortex (MFC) and the medial temporal lobe (MTL)2-5, but it remains unknown how these structures jointly implement flexible memory retrieval6,7. We recorded single neurons in MFC and MTL while human subjects switched8 between making memory- and categorization-based decisions9,10. Here we show that MFC rapidly implements changing task demands by utilizing different subspaces of neural activity during different types of decisions. In contrast, no effect of task demands was seen in the MTL. Choices requiring memory retrieval selectively engaged phase-locking of MFC neurons to field potentials in the theta-frequency band in the MTL. Choice-selective neurons in MFC signaled abstract yes-no decisions independent of behavioral response modality (button press or saccade). These findings reveal a novel mechanism for flexibly and selectively engaging memory retrieval11-14 and show that unlike perceptual decision-making15, memory-related information is only represented in frontal cortex when choices require it.

Science ◽  
2020 ◽  
Vol 368 (6498) ◽  
pp. eaba3313 ◽  
Author(s):  
Juri Minxha ◽  
Ralph Adolphs ◽  
Stefano Fusi ◽  
Adam N. Mamelak ◽  
Ueli Rutishauser

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.


2019 ◽  
Vol 121 (4) ◽  
pp. 1410-1427 ◽  
Author(s):  
Margaret Henderson ◽  
John T. Serences

Searching for items that are useful given current goals, or “target” recognition, requires observers to flexibly attend to certain object properties at the expense of others. This could involve focusing on the identity of an object while ignoring identity-preserving transformations such as changes in viewpoint or focusing on its current viewpoint while ignoring its identity. To effectively filter out variation due to the irrelevant dimension, performing either type of task is likely to require high-level, abstract search templates. Past work has found target recognition signals in areas of ventral visual cortex and in subregions of parietal and frontal cortex. However, target status in these tasks is typically associated with the identity of an object, rather than identity-orthogonal properties such as object viewpoint. In this study, we used a task that required subjects to identify novel object stimuli as targets according to either identity or viewpoint, each of which was not predictable from low-level properties such as shape. We performed functional MRI in human subjects of both sexes and measured the strength of target-match signals in areas of visual, parietal, and frontal cortex. Our multivariate analyses suggest that the multiple-demand (MD) network, including subregions of parietal and frontal cortex, encodes information about an object’s status as a target in the relevant dimension only, across changes in the irrelevant dimension. Furthermore, there was more target-related information in MD regions on correct compared with incorrect trials, suggesting a strong link between MD target signals and behavior. NEW & NOTEWORTHY Real-world target detection tasks, such as searching for a car in a crowded parking lot, require both flexibility and abstraction. We investigated the neural basis of these abilities using a task that required invariant representations of either object identity or viewpoint. Multivariate decoding analyses of our whole brain functional MRI data reveal that invariant target representations are most pronounced in frontal and parietal regions, and the strength of these representations is associated with behavioral performance.


2013 ◽  
Vol 25 (10) ◽  
pp. 1634-1648 ◽  
Author(s):  
Julie Duque ◽  
Etienne Olivier ◽  
Matthew Rushworth

Top–down control is critical to select goal-directed actions in changeable environments, particularly when several conflicting options compete for selection. In humans, this control system is thought to involve an inhibitory mechanism that suppresses the motor representation of unwanted responses to favor selection of the most appropriate action. Here, we aimed to evaluate the role of a region of the medial frontal cortex, the pre-SMA, in this form of inhibition by using a double coil TMS protocol combining repetitive TMS (rTMS) over the pre-SMA and a single-pulse TMS over the primary motor cortex (M1) during a visuomotor task that required participants to choose between a left or right button press according to an imperative cue. M1 stimulation allowed us to assess changes in motor excitability related to selected and nonselected (unwanted) actions, and rTMS was used to produce transient disruption of pre-SMA functioning. We found that when rTMS was applied over pre-SMA, inhibition of the nonselected movement representation was reduced. Importantly, this effect was only observed when the imperative cue produced a substantial amount of competition between the response alternatives. These results are consistent with previous studies pointing to a role of pre-SMA in competition resolution. In addition, our findings indicate that this function of pre-SMA involves the control of inhibitory influences directed at unwanted action representations.


2017 ◽  
Author(s):  
Linda M. Amarante ◽  
Marcelo S. Caetano ◽  
Mark Laubach

AbstractRodents lick to consume fluids. The reward value of ingested fluids is likely to be encoded by neuronal activity entrained to the lick cycle. Here, we investigated relationships between licking and reward signaling by the medial frontal cortex [MFC], a key cortical region for reward-guided learning and decision-making. Multi-electrode recordings of spike activity and field potentials were made in male rats as they performed an incentive contrast licking task. Rats received access to higher and lower value sucrose rewards over alternating 30 sec periods. They learned to lick persistently when higher value rewards were available and to suppress licking when lower value rewards were available. Spectral analysis of spikes and fields revealed evidence for reward value being encoded by the strength of phase-locking of a 6-12 Hz theta rhythm to the rats’ lick cycle. Recordings during the initial acquisition of the task found that the strength of phase-locking to the lick cycle was strengthened with experience. A modification of the task, with a temporal gap of 2 sec added between reward deliveries, found that the rhythmic signals persisted during periods of dry licking, a finding that suggests the MFC encodes either the value of the currently available reward or the vigor with which rats act to consume it. Finally, we found that reversible inactivations of the MFC in the opposite hemisphere eliminated the encoding of reward information. Together, our findings establish that a 6-12 Hz theta rhythm, generated by the rodent medial frontal cortex, is synchronized to rewarded actions.Significance StatementThe cellular and behavioral mechanisms of reward signaling by the medial frontal cortex [MFC] have not been resolved. We report evidence for a 6-12 Hz theta rhythm that is generated by the MFC and synchronized with ongoing consummatory actions. Previous studies of MFC reward signaling have inferred value coding upon temporally sustained activity during the period of reward consumption. Our findings suggest that MFC activity is temporally sustained due to the consumption of the rewarding fluids, and not necessarily the abstract properties of the rewarding fluid. Two other major findings were that the MFC reward signals persist beyond the period of fluid delivery and are generated by neurons within the MFC.


2020 ◽  
Vol 13 (6) ◽  
pp. 1689-1696
Author(s):  
Lina Willacker ◽  
Marco Roccato ◽  
Beril Nisa Can ◽  
Marianne Dieterich ◽  
Paul C.J. Taylor

1998 ◽  
Vol 80 (5) ◽  
pp. 2671-2687 ◽  
Author(s):  
Kae Nakamura ◽  
Katsuyuki Sakai ◽  
Okihide Hikosaka

Nakamura, Kae, Katsuyuki Sakai, and Okihide Hikosaka. Neuronal activity in medial frontal cortex during learning of sequential procedures. J. Neurophysiol. 80: 2671–2687, 1998. To study the role of medial frontal cortex in learning and memory of sequential procedures, we examined neuronal activity of the presupplementary motor area (pre-SMA) and supplementary motor area (SMA) while monkeys ( n = 2) performed a sequential button press task, “2 × 5 task.” In this paradigm, 2 of 16 (4 × 4 matrix) light-emitting diode buttons (called “set”) were illuminated simultaneously and the monkey had to press them in a predetermined order. A total of five sets (called “hyperset”) was presented in a fixed order for completion of a trial. We examined the neuronal activity of each cell using two kinds of hypersets: new hypersets that the monkey experienced for the first time for which he had to find the correct orders of button presses by trial-and-error and learned hypersets that the monkey had learned with extensive practice ( n = 16 and 10 for each monkey). To investigate whether cells in medial frontal cortex are involved in the acquisition of new sequences or execution of well-learned procedures, we examined three to five new hypersets and three to five learned hypersets for each cell. Among 345 task-related cells, we found 78 cells that were more active during performance of new hypersets than learned hypersets (new-preferring cells) and 18 cells that were more active for learned hypersets (learned-preferring cells). Among new-preferring cells, 33 cells showed a learning-dependent decrease of cell activity: their activity was highest at the beginning of learning and decreased as the animal acquired the correct response for each set with increasing reliability. In contrast, 11 learned-preferring cells showed a learning-dependent increase of neuronal activity. We found a difference in the anatomic distribution of new-preferring cells. The proportion of new-preferring cells was greater in the rostral part of the medial frontal cortex, corresponding to the pre-SMA, than the posterior part, the SMA. There was some trend that learned-preferring cells were more abundant in the SMA. These results suggest that the pre-SMA, rather than SMA, is more involved in the acquisition of new sequential procedures.


2017 ◽  
Author(s):  
Tomoki Kurikawa ◽  
Takashi Handa ◽  
Tomoki Fukai

AbstractDecision making obeys common neural mechanisms, but there is considerable variability in individuals’ decision making behavior particularly under uncertainty. How individual differences arise within common decision making brain systems is not known. Here, we explored this question in the medial frontal cortex (MFC) of rats performing a sensory-guided choice task. When rats trained on familiar stimuli were exposed to unfamiliar stimuli, choice responses varied significantly across individuals. We examined how variability in MFC neural processing could mediate this individual difference and constructed a network model to replicate this. Our model suggested that susceptibility of neural trajectories is a crucial determinant of the observed choice variability. The model predicted that trial-by-trial variability of trajectories are correlated with the susceptibility, and hence also correlated with the individual difference. This prediction was confirmed by experiment. Thus, our results suggest that variability in neural dynamics in MFC networks underlies individual differences in decision making.


1999 ◽  
Vol 82 (2) ◽  
pp. 1063-1068 ◽  
Author(s):  
Kae Nakamura ◽  
Katsuyuki Sakai ◽  
Okihide Hikosaka

To examine the role of the medial frontal cortex, supplementary motor area (SMA), and pre-SMA in the acquisition and control of sequential movements, we locally injected muscimol into 43 sites in the medial frontal cortex while monkeys (n = 2) performed a sequential button-press task. In this task, the monkey had to press two of 16 (4 × 4 matrix) buttons illuminated simultaneously in a predetermined order. A total of five pairs were presented in a fixed order for completion of a trial. To clarify the differential contribution of the medial frontal cortex for new acquisition and control of sequential movements, we used novel and learned sequences (that had been learned after extensive practice). We found that the number of errors increased for novel sequences, but not for learned sequences, after pre-SMA inactivations. A similar, but insignificant, trend was observed after SMA injections. The reaction time of button presses for both novel and learned sequences was prolonged by inactivations of both SMA and pre-SMA, with a trend for the effect to be larger for SMA inactivations. These findings suggest that the medial frontal cortex, especially pre-SMA, is related to the acquisition, rather than the storage or execution, of the correct order of button presses.


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