For things needing your attention: the role of neocortical gamma in sensory perception
Introduction
Neocortical oscillations in the gamma range (∼30–80 Hz) are hypothesized to benefit sensory processing [1], a prediction that has generated significant debate. A central hypothesis regarding gamma is that it can enhance the relay of sensory-evoked responses to downstream targets [2••, 3, 4••, 5, 6••], in turn enhancing the ability to detect stimuli at a behavioral level. The idea that gamma can act locally to facilitate sensory relay is conceptually distinct from another class of hypothesis, which posits that gamma oscillations are an essential feature of distributed sensory representations [7•, 8, 9]. Both classes of hypothesis have been contrasted with the view that only the rate of neocortical action potential firing influences signal relay, and that changes in action potential timing on the timescale of gamma — independent of changes in rate — should not benefit perception [10, 11, 12•]. As one noted physiologist quipped in support of this view, ‘gamma oscillations are the exhaust fumes of computation.’
These debates have been ongoing for many years, and until recently have entirely been made based on interpretations of correlative electrophysiological data. The advent of precise optogenetic control provides the opportunity to causally test whether gamma can enhance perceptual performance.
Section snippets
Discussing mechanism before considering meaning: synchronous fast-spiking activity is key to gamma emergence
Before discussing arguments for and against the utility of gamma, and how one might directly address these debates through causal manipulations, we first provide an overview of the circuit-level mechanisms driving this rhythm. The crucial role of fast-spiking interneurons (FS) in generating 30–80 Hz rhythms has been the focus of studies using electrophysiological observations, optogenetic perturbations, and computational models [2••, 3, 4••, 5, 13•, 14, 15, 16••, 17, 18, 19, 20, 21, 22, 23, 24].
Smoking gun? The current state of correlative evidence in favor of local gamma and gamma coherence
Correlative data have shown that local neocortical gamma oscillations are often present at an appropriate time to enhance processing. The allocation of attention to a specific position in space leads to increased gamma expression during stimulus presentation in the associated topographic position of area V4 [35••, 36, 37]. Recent brain–computer interface experiments have similarly shown that gamma can be expressed locally, on designated electrodes in an array, when monkeys are rewarded for
Signal relay to downstream targets is enhanced by local transformations driven by gamma
The dynamic ‘FS-gamma’ could enhance processing by locally conditioning representations — changing the timing or rate of sensory responses — in ways that increase the likelihood of a signal being relayed to a downstream target. Three main sub-hypotheses of this type have been offered.
First, the synchronous activity of FS has been predicted to enhance gain and/or sensitivity to excitatory input in the sensory responses of local pyramidal neurons, increasing their peak firing rates and thereby
Exhaust fume? The current state of correlative evidence against gamma
Several recent critiques of gamma have focused primarily on the view that fine timing is crucial to the effective relay of featural information. Studies in monkey primary visual neocortex (V1) have found that observed fluctuations in gamma frequencies across time and space would make it difficult for disparate cell assemblies to remain coherent in the gamma range, and more generally for the precise timing of such activity to carry meaningful signals about stimulus features. For example, the
Optogenetic drive of FS interneurons impacts sensory gain and temporal precision
As stated above, our consideration here of ‘gamma’ is focused on gamma driven by synchronous activity in FS interneurons, a mechanistic requirement that many view as the key step in emergence of meaningful neocortical gamma (e.g., gamma that can beneficially impact processing [2••, 3, 18]). Robust optogenetic drive of FS interneurons, typically targeted in neocortex through use of the parvalbumin (PV) reporter (in PV-cre mice), impacts local sensory encoding. Cardin and colleagues [4••] found
Optogenetic drive of FS interneurons can impair sensory detection
Activation of FS interneurons can suppress perceptual processing. Sachidhanandam and colleagues (2013) [66•] showed that high-frequency drive of FS (200 Hz) created strong hyperpolarization locally and suppressed perceptual detection of applied vibrissal stimulation. This suppression was observed when stimuli were applied both immediately following sensory onset, and during a ‘late phase’ component of the response. As discussed below, under specific conditions of sensory drive, Siegle et al.
Optogenetic drive of FS interneurons can enhance sensory detection
Other studies have found that, despite the net suppression of pyramidal firing rates observed with FS activation, stimulation of this cell class can enhance performance. Lee et al. (2012) observed that detection of a specific orientation of visual stimulation was enhanced by concurrent FS activation. In this study, the optogenetic stimulus was a continuous pulse of light lasting 5 seconds, and the temporal dynamics of activated FS were not measured [71•].
Siegle et al. (2014) used 40 Hz
FS-gamma as a reason for temporal transformations in sensory transduction and active sensing behaviors?
As mentioned above, Siegle et al. (2014) observed a negative impact of FS-gamma entrainment under certain conditions. By contrast to the enhancement described above when sensory input arrived at the optimal window of opportunity, a different phase of alignment, where sensory drive occurred just 5 milliseconds earlier, led to a decrement in detection probability, and other phases of alignment were not positively or negatively impacted. These findings suggest that the perceptual benefit of
Next steps in causal studies of gamma
The advent of optogenetics and other new methods that allow discrete causal control of specific cell types have rejuvenated reliance on causal manipulation as a form of key evidence in systems neuroscience [86]. The initial studies discussed here directly suggest a role for FS-gamma in local synchronization and/or local gain that promotes downstream relay of sensory information. A key future direction will be systematic testing of the specific impact of FS-gamma on synchrony and gain in select
Conflict of interest statement
Noting declared.
References and recommended reading
Papers of particular interest, published within the period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgments
This work was supported by a grant by the National Institute of Neurological Disorders and Stroke to CIM (2R56NS045130-10A1).
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2021, International Review of NeurobiologyCitation Excerpt :It was found that successful allocation of attention is characterized by elevated firing of medial PFC (mPFC) PV + interneurons, and increased gamma power. The enhanced gamma was signified by increased phase-locking of both PV + firing and firing of local excitatory neurons, with a strong phase concentration of the PV + spiking in the trough of the gamma cycle, consistent with the dynamics of gamma driven by fast-spiking PV + interneurons (Buzsáki & Wang, 2012; Pritchett, Siegle, Deister, & Moore, 2015). The gamma-synchronous PV + firing resulted in increased temporal precision and synchronization of the activities of local excitatory neurons, supporting the view that gamma rhythm supports the formation of neuronal assemblies with coordinated firing (Hasenstaub et al., 2005), a mechanism suggested to foster relay of relevant information and drive of activity in the proper targets with higher probability (Buzsáki & Watson, 2012; Salinas & Sejnowski, 2000; Salinas et al., 2001).
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2019, NeuronCitation Excerpt :This mechanism provides an explanation for the accompanying rate increase in sRS. Alternatively, rebound from FS inhibition may underlie sRS rate enhancement (Fellous et al., 2003; Knoblich et al., 2010; Pritchett et al., 2015; Tiesinga et al., 2004). Although the behavior of grnsFS is consistent with aforementioned gamma theories, this subtype shows a marked departure from the established relationship between FS and the LFP gamma (Cardin et al., 2009; Fries et al., 2001; Hasenstaub et al., 2005).
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2019, Behavioural Brain ResearchCitation Excerpt :The neuronal oscillatory can be divided into different frequency bands. For example, delta oscillation (0.5–3 Hz) was related to deep sleep [22]; theta oscillation (3.5–7 Hz) was related to cognitive function [23]; beta oscillation (13–30 Hz) was related to sensorimotor processing, attention, emotion, and cognitive control [24]; gamma oscillation (30–100 Hz) was thought to be involved in a number of sensory and cognitive responses [25]. It has been postulated that the effects of DBS may be due in part to promoting synchronization between brain regions involved in psychiatric disease [26], and this notion is supported by several studies in depression [11,27–29].