Coherent delta-band oscillations between cortical areas correlate with decision making

Nácher, Verónica; Ledberg, Anders; Deco, Gustavo; Romo, Ranulfo

doi:10.1073/pnas.1314681110

Cited by 138 publications

(106 citation statements)

References 41 publications

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“…We studied interactions between neuronal spike trains that were simultaneously recorded from five cortical areas in one trained monkey performing a somatosensory discrimination task (6). Recordings for the first monkey were performed in 13 independent sessions (n = 13).…”

Section: Resultsmentioning

confidence: 99%

Task-driven intra- and interarea communications in primate cerebral cortex

Campo

Martínez-García

Nácher

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Neural correlations during a cognitive task are central to study brain information processing and computation. However, they have been poorly analyzed due to the difficulty of recording simultaneous single neurons during task performance. In the present work, we quantified neural directional correlations using spike trains that were simultaneously recorded in sensory, premotor, and motor cortical areas of two monkeys during a somatosensory discrimination task. Upon modeling spike trains as binary time series, we used a nonparametric Bayesian method to estimate pairwise directional correlations between many pairs of neurons throughout different stages of the task, namely, perception, working memory, decision making, and motor report. We find that solving the task involves feedforward and feedback correlation paths linking sensory and motor areas during certain task intervals. Specifically, information is communicated by task-driven neural correlations that are significantly delayed across secondary somatosensory cortex, premotor, and motor areas when decision making takes place. Crucially, when sensory comparison is no longer requested for task performance, a major proportion of directional correlations consistently vanish across all cortical areas.vibrotactile discrimination | large-scale cortical networks | spike-train analysis | information theory | decision making T he problem of neural communication in the brain has been little explored traditionally due to the need for simultaneous recordings (1). The arrival of new techniques to record both neural population activity and single-neuron action potentials offers new prospects to study this problem (2, 3). Recently, population recordings have motivated a large number of works on multiunit interactions, including the study of interactions between local field potentials (LFPs) (4-6), LFPs and multiunit activity (5), and LFPs and neuronal spikes (7), but less attention has been paid to interactions between single-unit recordings (8). However, the analysis of simultaneous spike trains becomes critical because it is generally assumed that neurons are key units in distributing information across brain areas (9).An ideal paradigm to study neural communication is the somatosensory discrimination task designed by Romo and coworkers (10). In this task, a trained monkey discriminates the difference in frequency between two mechanical vibrations delivered sequentially to one fingertip (Fig. 1A). Essentially, the monkey must hold the first stimulus frequency (f 1) in working memory, must compare the second stimulus frequency (f 2) with the memory trace of f1 to form a decision of whether f 2 > f 1 or f 2 < f 1, and must postpone the decision until a sensory cue triggers the motor report (11). At the end of every trial, the monkey is rewarded with a drop of liquid for correct discriminations. Previous work on this task has analyzed how single-neuron responses across sensory and motor areas linearly correlate with stimuli and the decision report during the key stages of the ...

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Section: Resultsmentioning

confidence: 99%

Task-driven intra- and interarea communications in primate cerebral cortex

Campo

Martínez-García

Nácher

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…High levels of spike-field coherence reflect a tight coupling between the spiking of locally recorded units and particular frequency bands of the LFP (Pesaran et al 2002). It has been proposed that the rhythmic synchronization between spikes and LFPs may enhance the impact on downstream targets during sensory processing (Fries 2005; Fries et al 2001; Nacher et al 2013; Uhlhaas and Singer 2010). The finding of reduced baseline-corrected coherence in NRG1 (+/−) mutants thus indicates local deficits in neural synchrony and stimulus processing.…”

Section: Discussionmentioning

confidence: 99%

Altered resonance properties of somatosensory responses in mice deficient for the schizophrenia risk gene Neuregulin 1

Barz

Bessaïh²,

Abel

et al. 2015

Brain Struct Funct

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To reveal the neuronal underpinnings of sensory processing deficits in patients with schizophrenia, previous studies have investigated brain activity in response to sustained sensory stimulation at various frequencies. This paradigm evoked neural activity at the stimulation frequency and harmonics thereof. During visual and auditory stimulation that elicited enhanced or ‘resonant’ responses in healthy controls, patients with schizophrenia displayed reduced activity. The present study sought to elucidate the cellular basis of disease-related deficits in sensory resonance properties using mice heterozygous for the schizophrenia susceptibility gene Neuregulin 1 (NRG1). We applied repetitive whisker stimulation at 1–15 Hz, a range relevant to whisking behavior in mice, and measured cellular activity in the primary somatosensory cortex. At frequencies where control mice displayed enhancements in measures of response magnitude and precision, NRG1 (+/−) mutants showed reductions. Our results demonstrate for the first time a link between a mutation of a schizophrenia risk gene and altered neuronal resonance properties in sensory cortex.

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“…Needless to say, the delta entrainment across this large cortical circuit should be present during the SCT; however, the putaminal LFPs in monkeys did not show modulations in the delta band during this task. It is know that delta oscillations have their origin in thalamo-cortical interactions [103] and that play a critical role in the long-range interactions between cortical areas in behaving monkeys [104]. Hence, a possible explanation for this apparent discrepancy is that delta oscillations are part of the mechanism of information flow within cortical areas but not across the mCBGT circuit, which in turn could use interval tuning in the beta-and gamma-bands to represent the beat.…”

Section: Neurophysiology Of Rhythmic Behaviour In Monkeysmentioning

confidence: 99%

Finding the beat: a neural perspective across humans and non-human primates

Merchant¹,

Grahn

Trainor

et al. 2015

Phil. Trans. R. Soc. B

359

262

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One contribution of 12 to a theme Issue 'Biology, cognition and origins of musicality'. Humans possess an ability to perceive and synchronize movements to the beat in music ('beat perception and synchronization'), and recent neuroscientific data have offered new insights into this beat-finding capacity at multiple neural levels. Here, we review and compare behavioural and neural data on temporal and sequential processing during beat perception and entrainment tasks in macaques (including direct neural recording and local field potential (LFP)) and humans (including fMRI, EEG and MEG). These abilities rest upon a distributed set of circuits that include the motor cortico-basalganglia-thalamo-cortical (mCBGT) circuit, where the supplementary motor cortex (SMA) and the putamen are critical cortical and subcortical nodes, respectively. In addition, a cortical loop between motor and auditory areas, connected through delta and beta oscillatory activity, is deeply involved in these behaviours, with motor regions providing the predictive timing needed for the perception of, and entrainment to, musical rhythms. The neural discharge rate and the LFP oscillatory activity in the gamma-and beta-bands in the putamen and SMA of monkeys are tuned to the duration of intervals produced during a beat synchronization-continuation task (SCT). Hence, the tempo during beat synchronization is represented by different interval-tuned cells that are activated depending on the produced interval. In addition, cells in these areas are tuned to the serial-order elements of the SCT. Thus, the underpinnings of beat synchronization are intrinsically linked to the dynamics of cell populations tuned for duration and serial order throughout the mCBGT. We suggest that a cross-species comparison of behaviours and the neural circuits supporting them sets the stage for a new generation of neurally grounded computational models for beat perception and synchronization.

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Coherent delta-band oscillations between cortical areas correlate with decision making

Cited by 138 publications

References 41 publications

Task-driven intra- and interarea communications in primate cerebral cortex

Task-driven intra- and interarea communications in primate cerebral cortex

Altered resonance properties of somatosensory responses in mice deficient for the schizophrenia risk gene Neuregulin 1

Finding the beat: a neural perspective across humans and non-human primates

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