Temporal structure in neuronal activity during working memory in macaque parietal cortex

Abstract

A number of cortical structures are reported to have elevated single unit firing rates sustained throughout the memory period of a working memory task. How the nervous system forms and maintains these memories is unknown but reverberating neuronal network activity is thought to be important. We studied the temporal structure of single unit (SU) activity and simultaneously recorded local field potential (LFP) activity from area LIP in the inferior parietal lobe of two awake macaques during a memory-saccade task. Using multitaper techniques for spectral analysis, which play an important role in obtaining the present results, we find elevations in spectral power in a 50-90Hz (gamma) frequency band during the memory period in both SU and LFP activity. The activity is tuned to the direction of the saccade providing evidence for temporal structure that codes for movement plans during working memory. We also find SU and LFP activity are coherent during the memory period in the 50-90Hz gamma band and no consistent relation is present during simple fixation. Finally, we find organized LFP activity in a 15-25Hz frequency band that may be related to movement execution and preparatory aspects of the task. Neuronal activity could be used to control a neural prosthesis but SU activity can be hard to isolate with cortical implants. As the LFP is easier to acquire than SU activity, our finding of rich temporal structure in LFP activity related to movement planning and execution may accelerate the development of this medical application.Keywords: parietal, prosthesis, local field potential, gamma band, coherence, temporal structure.Pesaran et. al. 3Working memory is a brain system requiring the temporary storage and manipulation of information necessary for the performance of complex cognitive tasks (Baddeley, 1992). The neurophysiological basis of working memory is studied in non-human primates by recording neural activity during delayed-response tasks (Fuster, 1995). Cue-selective elevated single unit firing rates have been recorded during the delay period in many brain areas during different versions of the task (Fuster and Jervey, 1982;Bruce and Goldberg, 1985;Gnadt and Andersen, 1988;Miyashita and Chang, 1988;Funahashi et al., 1989;Koch and Fuster, 1989;Miller et al., 1996;Zhou and Fuster, 1996). How this neural activity is sustained is unknown but may be important to understanding the neural basis of working memory (Goldman-Rakic, 1995). Converging evidence points to the importance of a distributed recurrent neuronal network (Goldman-Rakic, 1988) and reverberating network activity has long been suggested as a possible mechanism for short-term memory (Lorente de No, 1938;Hebb, 1949;Amit, 1995;Seung, 1996;Wang, 1999).Measures with the potential to capture correlated neural activity on a millisecond time scale may be needed to resolve reverberating memory activity. The dynamical structure of neuronal activity has been the source of much interest as a temporal code (for a review see Singer and Gray (1995) ) however ...

Neural activities of tactile cross-modal working memory in humans: an event-related potential study

“…This is consistent with the idea that neural networks of the posterior association cortices specialize in particular modalities or aspects of sensory information (Fuster 2001;Fuster 2004). The activity of cells in the posterior parietal cortex (PPC) was shown to be correlated with working memory (Koch and Fuster, 1989;Quintana and Fuster, 1993;Iriki et al, 1996;Grunewald et al, 1999;Linden et al, 1999;Burton and Sinclair, 2000;Snyder et al, 2000;Andersen and Buneo, 2002;Pesaran et al, 2002;Constantinidis and Procyk, 2004). PPC was also shown in human imaging studies to be involved in crossmodal transfer of information between the tactile and visual representations (Hadjikhani and Roland, 1998;Saito et al, 2003).…”

Potentiation of Gamma Oscillatory Activity through Repetitive Transcranial Magnetic Stimulation of the Dorsolateral Prefrontal Cortex

“…The power of evoked and background components are then subtracted from the total power to provide an estimate of induced g-oscillatory activity (David et al, 2006). Although there are numerous reports that support a relationship between induced g-oscillatory activity and cognitive functions (Cho et al, 2006;Gray et al, 1989;Fries et al, 2001;Pesaran et al, 2002), a recent study showed that measures of induced g-activity may not only reflect synchronous neuronal activity, but also the activation of miniature saccadic eye movements (YuvalGreenberg et al, 2008). In their study, Yuval-Greenberg et al (2008) recorded eye movements simultaneously with EEG and found that induced g-activity was time locked to the onset and the rate of involuntary miniature saccades and thus reflects saccadic spike potentials rather than neuronal oscillations.…”

Statistical Issues in the Analysis of Neuronal Data

“…Our focus, in the remainder of this section, on estimation of (t) is not meant to imply that every analysis should begin with a time-domain representation of firing rate. In many situations, especially when oscillatory stimuli are used, frequency-domain analyses can produce valuable interpretations of the data (Brillinger 1992;Mechler et al 1998;Pesaran et al 2002).…”