Scientific Understanding of Consciousness
Working Memory Fronto-Parietal Synchronization
Science 23 November 2012: Vol. 338 no. 6110 pp. 1097-1100
Content-Specific Fronto-Parietal Synchronization During Visual Working Memory
R. F. Salazar, N. M. Dotson, S. L. Bressler, C. M. Gray
1Cell Biology and Neuroscience, Montana State University, Bozeman, MT 59717, USA.
2Center for Complex Systems and Brain Sciences, Florida Atlantic University, Boca Raton, FL 33431, USA.
Lateral prefrontal and posterior parietal cortical areas exhibit task-dependent activation during working memory tasks in humans and monkeys. Neurons in these regions become synchronized during attention-demanding tasks, but the contribution of these interactions to working memory is largely unknown. Using simultaneous recordings of neural activity from multiple areas in both regions, we find widespread, task-dependent, and content-specific synchronization of activity across the fronto-parietal network during visual working memory. The patterns of synchronization are prevalent among stimulus-selective neurons and are governed by influences arising in parietal cortex. These results indicate that short-term memories are represented by large-scale patterns of synchronized activity across the fronto-parietal network.
Working memory enables the short-term representation and utilization of behaviorally relevant information when that information is no longer available from the environment. How are such representations maintained in the brain? Extensive evidence demonstrates sustained activation in frontal and parietal areas during memory delay periods. Although the specific role of these activity patterns is not fully understood, theoretical, anatomical, and electrophysiological studies suggest that synchronous interactions among these cortical regions support working memory processes. While task-specific synchronization has been observed between prefrontal and parietal areas, its contribution to working memory is largely unknown. We tested the hypothesis that neuronal synchronization across the fronto-parietal network carries content-specific information that contributes directly to visual working memory. The pattern of fronto-parietal synchronization should thus vary as a function of the object held in memory.
We performed multi-electrode recordings of broadband neuronal activity [separated into unit activity and local field potentials (LFPs)] in prefrontal (PFC) and posterior parietal (PPC) cortices in two macaque monkeys while they performed an oculomotor, delayed match-to-sample task.
To determine which cortical areas engage in the synchronous memory-related activity, we sorted the fronto-parietal pairs showing significant delay-period CSI according to their respective cortical areas. The results reveal several notable findings. First, although our sample distribution was nonuniform, we found content-specific, fronto-parietal coherence among all sampled cortical areas. Second, the incidence of significant coherence selectivity varied widely (ranging from 4 to 50%) and occurred more often than expected from a uniform distribution (P < 0.05; randomization test) for both identity and location only among pairs involving the lateral bank of the intraparietal sulcus (i.e., areas PG and LIP). Thus, memory-related, fronto-parietal synchronization is a widespread process distributed across multiple cortical regions.
Our analysis suggests that fronto-parietal synchronization is governed by synaptic influences in PFC that arise in PPC. We used interareal spike-field coherence (SFC) measurements to evaluate this prediction, reasoning that this measure is indicative of directed synaptic influences. For each fronto-parietal pair, we calculated the SFC between spikes in one region and the LFP in the other during the delay period (1.0 to 1.8 s) and detected significant SFC as a function of frequency (P < 0.01). This revealed significant spectral peaks at frequencies between 10 and 30 Hz. We then calculated the mean incidence of significant SFC in the 12- to 22-Hz range for each cortical area in which the unit activity was recorded. The results showed a dominant PPC to PFC influence by demonstrating that significant SFC occurred more often in PPCunit–PFClfp pairs than PFCunit–PPClfp pairs (P < 0.05, KS test). The results showed a dominant PPC to PFC influence, as opposed to the relative phase results showing a PFC phase lead. This result supports previous findings that relative phase is not a reliable index of neural influence.
To further evaluate the contribution of unit response selectivity, we calculated the mutual information for firing rate as a function of time and, consistent with previous reports, found widespread selectivity during the sample and/or delay across both PFC and PPC areas.
Our findings demonstrate that fronto-parietal synchronization during visual working memory is widespread, task-dependent, and content-specific during the delay period. The patterns of synchronization are governed by influences arising in PPC and are prevalent among parietal neurons that display identity selectivity. These findings are consistent with other reports on the relationship between synchronization and performance in working memory tasks, the presence of fronto-parietal synchronization during memory-related search, and the spatial attention modulation of interareal coherence. Thus, although other cognitive processes—such as attention, anticipation, and motor planning—are likely to contribute to these effects, our findings demonstrate that short-term memories are represented as stimulus-specific patterns of synchronized activity that are widely distributed throughout the fronto-parietal network. This raises the question of how these patterns, their directional influences, spectral dynamics, and spatial distribution are modified by other working memory processes, such as retrieval, resistance to distraction, load, manipulation, and object-based attention. Other frequency bands have been associated with working memory, and abundant evidence indicates that other cortical areas contribute to these representations. A major challenge will be to elucidate the neuronal mechanisms underlying memory-related, fronto-parietal interactions and their relationship to different frequency bands and other cortical areas.
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