Prefrontal Task-Related Activity Representing Visual Cue Location or Saccade Direction in Spatial Working Memory Tasks

2002 ◽  
Vol 87 (1) ◽  
pp. 567-588 ◽  
Author(s):  
Kazuyoshi Takeda ◽  
Shintaro Funahashi
Keyword(s):  
Working Memory ◽  
Prefrontal Cortex ◽  
Spatial Working Memory ◽  
Delay Period ◽  
Neuron Activity ◽  
Delayed Response ◽  
Related Activity ◽  
Visual Cue ◽  
Response Period ◽  
Dorsolateral Prefrontal

To examine what kind of information task-related activity encodes during spatial working memory processes, we analyzed single-neuron activity in the prefrontal cortex while two monkeys performed two different oculomotor delayed-response (ODR) tasks. In the standard ODR task, monkeys were required to make a saccade to the cue location after a 3-s delay, whereas in the rotatory ODR (R-ODR) task, they were required to make a saccade 90° clockwise from the cue location after the 3-s delay. By comparing the same task-related activities in these two tasks, we could determine whether such activities encoded the location of the visual cue or the direction of the saccade. One hundred twenty one neurons exhibited task-related activity in relation to at least one task event in both tasks. Among them, 41 neurons exhibited directional cue-period activity, most of which encoded the location of the visual cue. Among 56 neurons with directional delay-period activity, 86% encoded the location of the visual cue, whereas 13% encoded the direction of the saccade. Among 57 neurons with directional response-period activity, 58% encoded the direction of the saccade, whereas 35% encoded the location of the visual cue. Most neurons whose response-period activity encoded the location of the visual cue also exhibited directional delay-period activity that encoded the location of the visual cue as well. The best directions of these two activities were identical, and most of these response-period activities were postsaccadic. Therefore this postsaccadic activity can be considered a signal to terminate unnecessary delay-period activity. Population histograms encoding the location of the visual cue showed tonic sustained activation during the delay period. However, population histograms encoding the direction of the saccade showed a gradual increase in activation during the delay period. These results indicate that the transformation from visual input to motor output occurs in the dorsolateral prefrontal cortex. The analysis using population histograms suggests that this transformation occurs gradually during the delay period.

Neuronal Activity Throughout the Primate Mediodorsal Nucleus of the Thalamus During Oculomotor Delayed-Responses. II. Activity Encoding Visual Versus Motor Signal

2004 ◽  
Vol 92 (3) ◽  
pp. 1756-1769 ◽  
Author(s):  
Yumiko Watanabe ◽  
Shintaro Funahashi
Keyword(s):  
Working Memory ◽  
Information Processing ◽  
Spatial Working Memory ◽  
Memory Task ◽  
Neuron Activity ◽  
Delayed Response ◽  
Related Activity ◽  
Response Period ◽  
Motor Information ◽  
Saccade Direction

We collected single-neuron activity from the mediodorsal (MD) nucleus of the thalamus, examined the information that was represented by task-related activity during performance of a spatial working memory task, and compared the present results with those obtained in the dorsolateral prefrontal cortex (DLPFC). We used two oculomotor delayed-response (ODR) tasks. In the ordinary ODR task, monkeys were required to make a memory-guided saccade to the location where a visual cue had been presented 3 s previously, whereas in the rotatory ODR task, they were required to make a memory-guided saccade 90° clockwise from the cue direction. By comparing the best directions of the same task-related activity between the two tasks, we could determine whether this activity represented the cue location or the saccade direction. All cue-period activity represented the cue location. In contrast, 56% of delay-period activity represented the cue location and 41% represented the saccade direction. Almost all response-period activity represented the saccade direction. These results indicate that task-related MD activity represents either visual or motor information, suggesting that the MD participates in sensory-to-motor information processing. However, a greater proportion of delay- and response-period activities represented the saccade direction in the MD than in the DLPFC, indicating that more MD neurons participate in prospective information processing than DLPFC neurons. These results suggest that although functional interactions between the MD and DLPFC are crucial to cognitive functions such as working memory, there is a difference in how the MD and DLPFC participate in these functions.

Drifts in Prefrontal and Parietal Neuronal Activity Influence Working Memory Judgments

2021 ◽  
Author(s):  
Sihai Li ◽  
Christos Constantinidis ◽  
Xue-Lian Qi
Keyword(s):  
Working Memory ◽  
Prefrontal Cortex ◽  
Dorsolateral Prefrontal Cortex ◽  
Posterior Parietal Cortex ◽  
Spatial Working Memory ◽  
Critical Role ◽  
Predictive Ability ◽  
Neuronal Firing ◽  
Delayed Response ◽  
Dorsolateral Prefrontal

Abstract The dorsolateral prefrontal cortex (dlPFC) plays a critical role in spatial working memory and its activity predicts behavioral responses in delayed response tasks. Here, we addressed if this predictive ability extends to other working memory tasks and if it is present in other brain areas. We trained monkeys to remember the location of a stimulus and determine whether a second stimulus appeared at the same location or not. Neurophysiological recordings were performed in the dorsolateral prefrontal cortex and posterior parietal cortex (PPC). We hypothesized that random drifts causing the peak activity of the network to move away from the first stimulus location and toward the location of the second stimulus would result in categorical errors. Indeed, for both areas, in nonmatching trials, when the first stimulus appeared in a neuron’s preferred location, the neuron showed significantly higher firing rates in correct than in error trials; and vice versa, when the first stimulus appeared at a nonpreferred location, activity in error trials was higher than in correct. The results indicate that the activity of both dlPFC and PPC neurons is predictive of categorical judgments of information maintained in working memory, and neuronal firing rate deviations are revealing of the contents of working memory.

Neuronal Activity Throughout the Primate Mediodorsal Nucleus of the Thalamus During Oculomotor Delayed-Responses. I. Cue-, Delay-, and Response-Period Activity

2004 ◽  
Vol 92 (3) ◽  
pp. 1738-1755 ◽  
Author(s):  
Yumiko Watanabe ◽  
Shintaro Funahashi
Keyword(s):  
Working Memory ◽  
Cognitive Functions ◽  
Spatial Working Memory ◽  
Memory Task ◽  
Delay Period ◽  
Mediodorsal Nucleus ◽  
Response Period ◽  
Dorsolateral Prefrontal ◽  
Oculomotor Responses ◽  
Higher Cognitive Functions

The thalamic mediodorsal nucleus (MD) has strong reciprocal connections with the dorsolateral prefrontal cortex (DLPFC), suggesting that the MD, like the DLPFC, participates in higher cognitive functions. To examine MD's participation in cognitive functions, we analyzed the characteristics of task-related activities sampled homogeneously from the MD while two monkeys performed a spatial working memory task using oculomotor responses. Of 141 task-related MD neurons, 26, 53, and 84% exhibited cue-, delay-, and response-period activity, respectively. Most of cue- and response-period activities showed phasic excitation, and most of delay-period activity showed tonic sustained activation. Among neurons with response-period activity, 74% exhibited presaccadic activity. Most cue-period, delay-period, and presaccadic activities were directional, whereas most postsaccadic activity was omni-directional. A significant contralateral bias in the best directions was present in cue-period and presaccadic activity. However, such bias was not present in delay-period activity, although most neurons had a best direction toward the contralateral visual field. We compared these characteristics with those observed in DLPFC neurons. Response-period activity was more frequently observed in the MD (84%) than in the DLPFC (56%). The directional selectivity and bias of task-related activities and the ratios of pre- and postsaccadic activities were different between MD and DLPFC. These results indicate that the MD participates in higher cognitive functions such as spatial working memory. However, the manner in which these two structures participate in these processes differs, in that the MD participates more in motor control aspects compared with the DLPFC.

Activity in Human Frontal Cortex Associated with Spatial Working Memory and Saccadic Behavior

2000 ◽  
Vol 12 (supplement 2) ◽  
pp. 2-14 ◽  
Author(s):  
Bradley R. Postle ◽  
Jeffrey S. Berger ◽  
Alexander M. Taich ◽  
Mark D'Esposito
Keyword(s):  
Working Memory ◽  
Frontal Cortex ◽  
Signal Intensity ◽  
Spatial Working Memory ◽  
Delay Period ◽  
Delayed Response ◽  
Related Activity ◽  
Memory Condition ◽  
Fmri Signal ◽  
Spatio Temporal

We examined, with event-related fMRI, two hypotheses about the organization of human working memory function in frontal cortex: (1) that a region immediately anterior to the frontal eye fields (FEF) (superior frontal cortex, SFC) is specialized for spatial working memory (Courtney, et al., 1998); and (2) that dorsolateral prefrontal cortex (PFC) plays a privileged role in the manipulation of spatial stimuli held in working memory (Owen, et al., 1996; Petrides 1994). Our delayed-response task featured 2-D arrays of irregularly arranged squares that were highlighted serially in a random sequence. The Forward Memory condition required maintenance of the spatio-temporal sequence, the Manipulate Memory condition required reordering this sequence into a new spatially defined order, the Guided Saccade condition required saccades to highlighted squares in the array, but no memory, and the Free Saccade condition required self-paced, horizontal saccades. The comparison of fMRI signal intensity associated with 2-D saccade generation (Guided Saccades) versus fMRI signal intensity associated with the delay period of the working memorials condition revealed no evidence for greater working memory-related activity than saccade-related activity in SFC in any individual subject, nor at the level of the group, and greater 2-D saccade than delay-period activity in three of five subjects. These results fail to support the hypothesis that spatial working memory-related activity is represented preferentially in a region of SFC anterior to the FEF (Courtney, et al., 1998). The comparison of maintenance versus manipulation of spatio-temporal information in working memory revealed significantly greater activity associated with the latter in dorsolateral PFC, but not in ventrolateral PFC or in SFC. These results suggest that the delay-related function of SFC is limited to the maintenance of spatial information, and that this region does not support the nonmnemonic executive control functions supported by dorsolateral PFC. These results also indicate that the preferential recruitment of dorsolateral PFC for the manipulation of information held in working memory applies to tasks employing spatial stimuli, as well as to tasks employing verbal stimuli (D'Esposito, et al., 1999); Petrides et al., 1993; Postle et al., 1999).

scholarly journals Prefrontal and Parietal Attractor Networks Mediate Working Memory Judgments

2020 ◽  
Author(s):  
Sihai Li ◽  
Christos Constantinidis ◽  
Xue-Lian Qi
Keyword(s):  
Working Memory ◽  
Prefrontal Cortex ◽  
Dorsolateral Prefrontal Cortex ◽  
Critical Role ◽  
Memory Task ◽  
Delayed Response ◽  
Persistent Activity ◽  
Neural Basis ◽  
Brain Areas ◽  
Dorsolateral Prefrontal

ABSTRACTThe dorsolateral prefrontal cortex plays a critical role in spatial working memory and its activity predicts behavioral responses in delayed response tasks. Here we addressed whether this predictive ability extends to categorical judgments based on information retained in working memory, and is present in other brain areas. We trained monkeys in a novel, Match-Stay, Nonmatch-Go task, which required them to observe two stimuli presented in sequence with an intervening delay period between them. If the two stimuli were different, the monkeys had to saccade to the location of the second stimulus; if they were the same, they held fixation. Neurophysiological recordings were performed in areas 8a and 46 of the dlPFC and 7a and lateral intraparietal cortex (LIP) of the PPC. We hypothesized that random drifts causing the peak activity of the network to move away from the first stimulus location and towards the location of the second stimulus would result in categorical errors. Indeed, for both areas, when the first stimulus appeared in a neuron’s preferred location, the neuron showed significantly higher firing rates in correct than in error trials. When the first stimulus appeared at a nonpreferred location and the second stimulus at a preferred, activity in error trials was higher than in correct. The results indicate that the activity of both dlPFC and PPC neurons is predictive of categorical judgments of information maintained in working memory, and the magnitude of neuronal firing rate deviations is revealing of the contents of working memory as it determines performance.SIGNIFICANCE STATEMENTThe neural basis of working memory and the areas mediating this function is a topic of controversy. Persistent activity in the prefrontal cortex has traditionally been thought to be the neural correlate of working memory, however recent studies have proposed alternative mechanisms and brain areas. Here we show that persistent activity in both the dorsolateral prefrontal cortex and posterior parietal cortex predicts behavior in a working memory task that requires a categorical judgement. Our results offer support to the idea that a network of neurons in both areas act as an attractor network that maintains information in working memory, which informs behavior.

scholarly journals Stable population coding for working memory coexists with heterogeneous neural dynamics in prefrontal cortex

2016 ◽  
Vol 114 (2) ◽  
pp. 394-399 ◽  
Author(s):  
John D. Murray ◽  
Alberto Bernacchia ◽  
Nicholas A. Roy ◽  
Christos Constantinidis ◽  
Ranulfo Romo ◽  
...  
Keyword(s):  
Working Memory ◽  
Prefrontal Cortex ◽  
Neural Circuit ◽  
Temporal Dynamics ◽  
Population Level ◽  
Population Coding ◽  
Neural Dynamics ◽  
Stable Population ◽  
Neuron Activity ◽  
Delayed Response

Working memory (WM) is a cognitive function for temporary maintenance and manipulation of information, which requires conversion of stimulus-driven signals into internal representations that are maintained across seconds-long mnemonic delays. Within primate prefrontal cortex (PFC), a critical node of the brain’s WM network, neurons show stimulus-selective persistent activity during WM, but many of them exhibit strong temporal dynamics and heterogeneity, raising the questions of whether, and how, neuronal populations in PFC maintain stable mnemonic representations of stimuli during WM. Here we show that despite complex and heterogeneous temporal dynamics in single-neuron activity, PFC activity is endowed with a population-level coding of the mnemonic stimulus that is stable and robust throughout WM maintenance. We applied population-level analyses to hundreds of recorded single neurons from lateral PFC of monkeys performing two seminal tasks that demand parametric WM: oculomotor delayed response and vibrotactile delayed discrimination. We found that the high-dimensional state space of PFC population activity contains a low-dimensional subspace in which stimulus representations are stable across time during the cue and delay epochs, enabling robust and generalizable decoding compared with time-optimized subspaces. To explore potential mechanisms, we applied these same population-level analyses to theoretical neural circuit models of WM activity. Three previously proposed models failed to capture the key population-level features observed empirically. We propose network connectivity properties, implemented in a linear network model, which can underlie these features. This work uncovers stable population-level WM representations in PFC, despite strong temporal neural dynamics, thereby providing insights into neural circuit mechanisms supporting WM.

Isodirectional Tuning of Adjacent Interneurons and Pyramidal Cells During Working Memory: Evidence for Microcolumnar Organization in PFC

1999 ◽  
Vol 81 (4) ◽  
pp. 1903-1916 ◽  
Author(s):  
Srinivas G. Rao ◽  
Graham V. Williams ◽  
Patricia S. Goldman-Rakic
Keyword(s):  
Working Memory ◽  
Prefrontal Cortex ◽  
Receptive Fields ◽  
Pyramidal Cells ◽  
Delayed Response ◽  
Cellular Mechanisms ◽  
Threshold Response ◽  
Dorsolateral Prefrontal ◽  
Fast Spiking ◽  
Spatially Oriented

Isodirectional tuning of adjacent interneurons and pyramidal cells during working memory: evidence for microcolumnar organization in PFC. Studies on the cellular mechanisms of working memory demonstrated that neurons in dorsolateral prefrontal cortex (dPFC) exhibit directionally tuned activity during an oculomotor delayed response. To determine the particular contributions of pyramidal cells and interneurons to spatial tuning in dPFC, we examined both individually and in pairs the tuning properties of regular-spiking (RS) and fast-spiking (FS) units that represent putative pyramidal cells and interneurons, respectively. Our main finding is that FS units possess spatially tuned sensory, motor, and delay activity (i.e., “memory fields”) similar to those found in RS units. Furthermore, when recorded simultaneously at the same site, the majority of neighboring neurons, whether FS or RS, displayed isodirectional tuning, i.e., they shared very similar tuning angles for the sensory and delay phases of the task. As the trial entered the response phase of the task, many FS units shifted their direction of tuning and became cross-directional to adjacent RS units by the end of the trial. These results establish that a large part of inhibition in prefrontal cortex is spatially oriented rather than being untuned and simply regulating the threshold response of pyramidal cell output. Moreover, the isodirectional tuning between adjacent neurons supports a functional microcolumnar organization in dPFC for spatial memory fields similar to that found in other areas of cortex for sensory receptive fields.

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