Adaptation-induced synchronization in laminar cortical circuits

Abstract

A fundamental feature of information processing in neocortex is the ability of individual neurons to adapt to changes in incoming stimuli. It is increasingly being understood that cortical adaptation is a phenomenon that requires network interactions. The fact that the structure of local networks depends critically on cortical layer raises the possibility that adaptation could induce specific effects in different layers. Here we show that brief exposure (300 ms) to a stimulus of fixed orientation modulates the strength of synchronization between individual neurons and local population activity in the gamma-band frequency (30-80 Hz) in macaque primary visual cortex (V1) and influences the ability of individual neurons to encode stimulus orientation. Using laminar probes, we found that although stimulus presentation elicits a large increase in the gamma synchronization of rhythmic neuronal activity in the input (granular) layers of V1, adaptation caused a pronounced increase in synchronization in the cortical output (supragranular) layers. The increase in gamma synchronization after adaptation was significantly correlated with an improvement in neuronal orientation discrimination performance only in the supragranular layers. Thus, synchronization between the spiking activity of individual neurons and their local population may enhance sensory coding to optimize network processing across laminar circuits.A fundamental issue in our understanding of brain circuits is how networks in different layers of the cerebral cortex encode information. Cortical layers are ubiquitous structures throughout neocortex (1, 2) that consist of highly recurrent local networks that communicate among each other to possibly influence the information encoded in population activity. In recent years, significant progress has been made in our understanding of the differences in response properties of neurons across cortical layers (3, 4), yet there is still a great deal to learn about whether and how neuronal populations encode information in a layerspecific manner. A measure of the activity of a local population (or ensemble) of neurons (5) is captured by local field potentials (LFPs), which are composed of low-frequency extracellular voltage fluctuations, including local excitatory and inhibitory intracortical inputs (6) believed to originate from within 250-500 μm of the recording site (7,8). In visual cortex, it has been found that neuronal groups exhibit strong responses in the gammaband frequency (30-80 Hz) (9-11) and that single neurons synchronize their responses with the local population activity (12, 13). Synchronization in visual cortex, particularly in the gammaband, has been found to be critically involved in sensory processing (9,11,14), grouping (9, 11; but see refs. 15-17), attention (10,(18)(19)(20), working memory (5), and behavioral reaction times (20). The results of these studies support the hypothesis that efficient information transmission would occur whenever two networks are synchronous in their excitability peaks, wh...

Stimulus repetition affects both strength and synchrony of macaque inferior temporal cortical activity

“…The effects of adaptation on synchronized IT activity differ from recent reports of an enhancement of synchronization in alpha to gamma frequencies in the supragranular layers in V1 (Hansen and Dragoi 2011) and around 60 Hz in V4 (Wang et al 2011). Stimulus repetition synchronization effects, like attention effects (Chalk et al 2010), may differ between areas, which is possible since synchronization depends on circuit, synaptic, and cellular (e.g., ion channels) properties (Wang 2010).…”

“…Previous studies in early visual cortical areas suggested that coherence can depend on the lamina (Bollimunta et al 2008;Buffalo et al 2011;Hansen and Dragoi 2011;Maier et al 2010) and decreases with interelectrode distance (Hansen and Dragoi 2011;Maier et al 2010;Ray and Maunsell 2011). We have already noted that differences between the two animals in some of the repetition effects diminish when one accepts deeper recordings in monkey K compared with monkey G. Changes in coherence effects with depth may also explain other observed interanimal differences.…”

“…In both monkeys LFP-LFP coherences that involved deep recording sites showed suppression of the synchronization in the beta and low gamma bands, suggesting that coherence effects are layer dependent. Layerdependent differences in coherences have also been observed for attention (Buffalo et al 2011) and fast adaptation effects (Hansen and Dragoi 2011) in early visual cortex.…”

“…2010). Recent studies in macaque areas V1 and V4 reported enhanced synchronized activity following adaptation with a short ISI (100 ms) for particular frequency bands, including the gamma band (Hansen and Dragoi 2011;Wang et al 2011). Furthermore, Gutnisky and Dragoi (2008) found decreased trial-to-trial spiking activity correlations following brief adaptation in V1, but such an effect was unreliable in V4 (Wang et al 2011).…”

Opposite Adaptive Processing of Stimulus Intensity in Two Major Nuclei of the Somatosensory Brainstem

“…In the somatosensory system, adaptation profoundly shapes the neuronal response along the pathways conveying tactile information to the cortex (Wang et al, 2010;Hansen and Dragoi, 2011). The major mechanism proposed for adaptation in this system is short-term synaptic depression (STD; Tsodyks and Markram, 1997;Chung et al, 2002), in which the response gradually adapts due to the limited synaptic resources and their slow recovery.…”