Temporal Correlation Mechanisms and Their Role in Feature Selection: A Single-Unit Study in Primate Somatosensory Cortex

Gomez‐Ramirez, Manuel; Trzcinski, Natalie K.; Mihalaş, Ştefan; Niebur, Ernst; Hsiao, Steven S.

doi:10.1371/journal.pbio.1002004

Cited by 18 publications

(19 citation statements)

References 56 publications

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“…1A). The single-unit data for this study have previously been used in other studies that addressed the link between firing rate and behavior after the motion pulse occurred Farah et al, 2014). Here we instead focused on the period leading up to the motion pulse.…”

Section: Resultsmentioning

confidence: 99%

“…Behavioral task. The data for this study have been previously described Farah et al, 2014). Two male monkeys (Macaca mulatta) were trained to perform a coherent motion pulse detection task outlined in Figure 1C.…”

Section: Methodsmentioning

confidence: 99%

“…In comparison, correlations between neurons on much shorter timescales (measured on a single trial and referred to as synchrony or spike-time correlation) can affect information coding, but their origin and impact on behavior remain a focus of investigation (Singer and Gray, 1995;Steinmetz et al, 2000;Fries et al, 2001a;Kimpo et al, 2003;Thiele and Stoner, 2003;Hirabayashi and Miyashita, 2005;Palanca and DeAngelis, 2005;Mitchell et al, 2009;Huang and Lisberger, 2013;Gomez-Ramirez et al, 2014). For example, attention has been reported to reduce across-trial noise correlations Maunsell, 2009, 2010), but increase spike-time correlations (Steinmetz et al, 2000;Fries et al, 2001a).…”

Section: Introductionmentioning

confidence: 99%

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The Magnitude, But Not the Sign, of MT Single-Trial Spike-Time Correlations Predicts Motion Detection Performance

et al. 2018

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Spike-time correlations capture the short timescale covariance between the activity of neurons on a single trial. These correlations can significantly vary in magnitude and sign from trial to trial, and have been proposed to contribute to information encoding in visual cortex. While monkeys performed a motion-pulse detection task, we examined the behavioral impact of both the magnitude and sign of single-trial spike-time correlations between two nonoverlapping pools of middle temporal (MT) neurons. We applied three single-trial measures of spike-time correlation between our multiunit MT spike trains (Pearson's, absolute value of Pearson's, and mutual information), and examined the degree to which they predicted a subject's performance on a trial-by-trial basis. We found that on each trial, positive and negative spike-time correlations were almost equally likely, and, once the correlational sign was accounted for, all three measures were similarly predictive of behavior. Importantly, just before the behaviorally relevant motion pulse occurred, single-trial spike-time correlations were as predictive of the performance of the animal as single-trial firing rates. While firing rates were positively associated with behavioral outcomes, the presence of either strong positive or negative correlations had a detrimental effect on behavior. These correlations occurred on short timescales, and the strongest positive and negative correlations modulated behavioral performance by ∼9%, compared with trials with no correlations. We suggest a model where spike-time correlations are associated with a common noise source for the two MT pools, which in turn decreases the signal-to-noise ratio of the integrated signals that drive motion detection. Previous work has shown that spike-time correlations occurring on short timescales can affect the encoding of visual inputs. Although spike-time correlations significantly vary in both magnitude and sign across trials, their impact on trial-by-trial behavior is not fully understood. Using neural recordings from area MT (middle temporal) in monkeys performing a motion-detection task using a brief stimulus, we found that both positive and negative spike-time correlations predicted behavioral responses as well as firing rate on a trial-by-trial basis. We propose that strong positive and negative spike-time correlations decreased behavioral performance by reducing the signal-to-noise ratio of integrated MT neural signals.

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Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The Magnitude, But Not the Sign, of MT Single-Trial Spike-Time Correlations Predicts Motion Detection Performance

et al. 2018

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“…Attending to the tactile information of a bimodal visuo-tactile stimulus increased the firing rates of neurons in the primary (SI) and secondary (SII) somatosensory cortices as compared to the case when attention was directed to the visual information (Hsiao, O'Shaughnessy, & Johnson, 1993). When attention had to be directed to one of two tactile features (orientation and vibratory frequency) higher firing rates were observed in SII neurons selective for this specific feature (Gomez-Ramirez, Trzcinski, Mihalas, Niebur, & Hsiao, 2014). Furthermore, it has been shown that tactile attention increased synchronization of neural spiking activity of feature selective cells in the SII, which correlated with performance (Gomez-Ramirez et al, 2014).…”

Section: Introductionmentioning

confidence: 93%

Top-down modulation of shape and roughness discrimination in active touch by covert attention

Metzger

Mueller

Fiehler

et al. 2018

Atten Percept Psychophys

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Due to limitations in perceptual processing, information relevant to momentary task goals is selected from the vast amount of available sensory information by top-down mechanisms (e.g. attention) that can increase perceptual performance. We investigated how covert attention affects perception of 3D objects in active touch. In our experiment, participants simultaneously explored the shape and roughness of two objects in sequence, and were told afterwards to compare the two objects with regard to one of the two features. To direct the focus of covert attention to the different features we manipulated the expectation of a shape or roughness judgment by varying the frequency of trials for each task (20%, 50%, 80%), then we measured discrimination thresholds. We found higher discrimination thresholds for both shape and roughness perception when the task was unexpected, compared to the conditions in which the task was expected (or both tasks were expected equally). Our results suggest that active touch perception is modulated by expectations about the task. This implies that despite fundamental differences, active and passive touch are affected by feature selective covert attention in a similar way.

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“…All other points were assigned a zero value. We convolved MUA activity with an asymmetric Gaussian filter (30ms duration, with a rising slope = 19.91mV/s) to derive instantaneous MUA (Gomez-Ramirez et al, 2014). Individual observations used in the statistics comprised averaged activity between -1500ms and -500ms prior to the onset of the tactile stimulus.…”

Section: Analysesmentioning

confidence: 99%

The BioLuminescent-OptoGenetic in vivo Response to Coelenterazine is Proportional, Sensitive and Specific in Neocortex

Gomez‐Ramirez

Friedman

et al. 2019

Preprint

Self Cite

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BioLuminescent (BL) light production can modulate neural activity and behavior through coexpressed OptoGenetic (OG) elements, an approach termed 'BL-OG'. Yet, the relationship between BL-OG effects and bioluminescent photon emission has not been characterized in vivo.Further, the degree to which BL-OG effects strictly depend on optogenetic mechanisms driven by bioluminescent photons is unknown. Crucial to every neuromodulation method is whether the activator shows a dynamic concentration range driving robust, selective, and non-toxic effects.We systematically tested the effects of four key components of the BL-OG mechanism (luciferin, oxidized luciferin, luciferin vehicle, and bioluminescence), and compared these against effects induced by the Luminopsin-3 (LMO3) BL-OG molecule, a fusion of slow burn Gaussia luciferase (sbGLuc) and Volvox ChannelRhodopsin-1 (VChR1). We performed combined bioluminescence imaging and electrophysiological recordings while injecting specific doses of Coelenterazine (substrate for sbGluc), Coelenteramide (CTM, the oxidized product of CTZ), or CTZ vehicle. CTZ robustly drove activity in mice expressing LMO3, with photon production proportional to firing rate. In contrast, low and moderate doses of CTZ, CTM, or vehicle did not modulate activity in mice that did not express LMO3. We also failed to find bioluminescence effects on neural activity in mice expressing an optogenetically non-sensitive LMO3 variant. We observed weak responses to the highest dose of CTZ in control mice, but these effects were significantly smaller than those observed in the LMO3 group. These results show that in neocortex in vivo, there is a large CTZ range wherein BL-OG effects are specific to its active chemogenetic mechanism.

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Temporal Correlation Mechanisms and Their Role in Feature Selection: A Single-Unit Study in Primate Somatosensory Cortex

Abstract: How neurons pay attention Top-down selective attention mediates feature selection by reducing the noise correlations in neural populations and enhancing the synchronized activity across subpopulations that encode the relevant features of sensory stimuli.

Cited by 18 publications

References 56 publications

The Magnitude, But Not the Sign, of MT Single-Trial Spike-Time Correlations Predicts Motion Detection Performance

The Magnitude, But Not the Sign, of MT Single-Trial Spike-Time Correlations Predicts Motion Detection Performance

Top-down modulation of shape and roughness discrimination in active touch by covert attention

The BioLuminescent-OptoGenetic in vivo Response to Coelenterazine is Proportional, Sensitive and Specific in Neocortex

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