ABSTRACT
The brain is organized hierarchically to process sensory signals. But, how do functional connections within and across areas contribute to this hierarchical order? We addressed this problem in the thalamocortical network, while monkeys detected vibrotactile stimulus. During this task, we quantified neural variability and directed functional connectivity in simultaneously recorded neurons sharing the cutaneous receptive field within and across VPL and areas 3b and 1. Before stimulus onset, VPL and area 3b exhibited similar fast dynamics while area 1 showed slower timescales. During the stimulus presence, inter-trial neural variability increased along the network VPL-3b-1 while VPL established two main feedforward pathways with areas 3b and 1 to process the stimulus. This lower variability of VPL and area 3b was found to regulate feedforward thalamocortical pathways. Instead, intra-cortical interactions were only anticipated by higher intrinsic timescales in area 1. Overall, our results provide evidence of hierarchical functional roles along the thalamocortical network.
ABSTRACT
How does the brain simultaneously process signals that bring complementary information, like raw sensory signals and their transformed counterparts, without any disruptive interference? Contemporary research underscores the brain's adeptness in using decorrelated responses to reduce such interference. Both neurophysiological findings and artificial neural networks support the notion of orthogonal representation for signal differentiation and parallel processing. Yet, where, and how raw sensory signals are transformed into more abstract representations remains unclear. Using a temporal pattern discrimination task in trained monkeys, we revealed that the second somatosensory cortex (S2) efficiently segregates faithful and transformed neural responses into orthogonal subspaces. Importantly, S2 population encoding for transformed signals, but not for faithful ones, disappeared during a nondemanding version of this task, which suggests that signal transformation and their decoding from downstream areas are only active on-demand. A mechanistic computation model points to gain modulation as a possible biological mechanism for the observed context-dependent computation. Furthermore, individual neural activities that underlie the orthogonal population representations exhibited a continuum of responses, with no well-determined clusters. These findings advocate that the brain, while employing a continuum of heterogeneous neural responses, splits population signals into orthogonal subspaces in a context-dependent fashion to enhance robustness, performance, and improve coding efficiency.
Subject(s)
Macaca mulatta , Somatosensory Cortex , Animals , Somatosensory Cortex/physiology , Models, Neurological , MaleABSTRACT
The dorsal premotor cortex (DPC) has classically been associated with a role in preparing and executing the physical motor variables during cognitive tasks. While recent work has provided nuanced insights into this role, here we propose that DPC also participates more actively in decision-making. We recorded neuronal activity in DPC while two trained monkeys performed a vibrotactile categorization task, utilizing two partially overlapping ranges of stimulus values that varied on two physical attributes: vibrotactile frequency and amplitude. We observed a broad heterogeneity across DPC neurons, the majority of which maintained the same response patterns across attributes and ranges, coding in the same periods, mixing temporal and categorical dynamics. The predominant categorical signal was maintained throughout the delay, movement periods and notably during the intertrial period. Putting the entire population's data through two dimensionality reduction techniques, we found strong temporal and categorical representations without remnants of the stimuli's physical parameters. Furthermore, projecting the activity of one population over the population axes of the other yielded identical categorical and temporal responses. Finally, we sought to identify functional subpopulations based on the combined activity of all stimuli, neurons, and time points; however, we found that single-unit responses mixed temporal and categorical dynamics and couldn't be clustered. All these point to DPC playing a more decision-related role than previously anticipated.
Subject(s)
Motor Cortex , Motor Cortex/physiology , Neurons/physiology , Movement/physiologyABSTRACT
Do sensory cortices process more than one sensory modality? To answer these questions, scientists have generated a wide variety of studies at distinct space-time scales in different animal models, and often shown contradictory conclusions. Some conclude that this process occurs in early sensory cortices, but others that this occurs in areas central to sensory cortices. Here, we sought to determine whether sensory neurons process and encode physical stimulus properties of different modalities (tactile and acoustic). For this, we designed a bimodal detection task where the senses of touch and hearing compete from trial to trial. Two Rhesus monkeys performed this novel task, while neural activity was recorded in areas 3b and 1 of the primary somatosensory cortex (S1). We analyzed neurons' coding properties and variability, organizing them by their receptive field's position relative to the stimulation zone. Our results indicate that neurons of areas 3b and 1 are unimodal, encoding only the tactile modality in both the firing rate and variability. Moreover, we found that neurons in area 3b carried more information about the periodic stimulus structure than those in area 1, possessed lower response and coding latencies, and had a lower intrinsic time scale. In sum, these differences reveal a hidden processing-based hierarchy. Finally, using a powerful nonlinear dimensionality reduction algorithm, we show that the activity from areas 3b and 1 can be separated, establishing a clear division in the functionality of these two subareas of S1.
Subject(s)
Somatosensory Cortex , Touch Perception , Animals , Somatosensory Cortex/physiology , Touch Perception/physiology , Touch , Parietal Lobe , Sensory Receptor CellsABSTRACT
Little is known about how dopamine (DA) neuron firing rates behave in cognitively demanding decision-making tasks. Here, we investigated midbrain DA activity in monkeys performing a discrimination task in which the animal had to use working memory (WM) to report which of two sequentially applied vibrotactile stimuli had the higher frequency. We found that perception was altered by an internal bias, likely generated by deterioration of the representation of the first frequency during the WM period. This bias greatly controlled the DA phasic response during the two stimulation periods, confirming that DA reward prediction errors reflected stimulus perception. In contrast, tonic dopamine activity during WM was not affected by the bias and did not encode the stored frequency. More interestingly, both delay-period activity and phasic responses before the second stimulus negatively correlated with reaction times of the animals after the trial start cue and thus represented motivated behavior on a trial-by-trial basis. During WM, this motivation signal underwent a ramp-like increase. At the same time, motivation positively correlated with accuracy, especially in difficult trials, probably by decreasing the effect of the bias. Overall, our results indicate that DA activity, in addition to encoding reward prediction errors, could at the same time be involved in motivation and WM. In particular, the ramping activity during the delay period suggests a possible DA role in stabilizing sustained cortical activity, hypothetically by increasing the gain communicated to prefrontal neurons in a motivation-dependent way.
Subject(s)
Dopamine/pharmacology , Memory, Short-Term/physiology , Motivation/physiology , Reward , Animals , Behavior, Animal/physiology , Dopaminergic Neurons/physiology , Male , Mesencephalon/physiologyABSTRACT
A crucial role of cortical networks is the conversion of sensory inputs into perception. In the cortical somatosensory network, neurons of the primary somatosensory cortex (S1) show invariant sensory responses, while frontal lobe neuronal activity correlates with the animal's perceptual behavior. Here, we report that in the secondary somatosensory cortex (S2), neurons with invariant sensory responses coexist with neurons whose responses correlate with perceptual behavior. Importantly, the vast majority of the neurons fall along a continuum of combined sensory and categorical dynamics. Furthermore, during a non-demanding control task, the sensory responses remain unaltered while the sensory information exhibits an increase. However, perceptual responses and the associated categorical information decrease, implicating a task context-dependent processing mechanism. Conclusively, S2 neurons exhibit intriguing dynamics that are intermediate between those of S1 and frontal lobe. Our results contribute relevant evidence about the role that S2 plays in the conversion of touch into perception.
Subject(s)
Macaca mulatta/physiology , Neurons/physiology , Sensory Receptor Cells/physiology , Somatosensory Cortex/physiology , Touch Perception/physiology , Algorithms , Animals , Frontal Lobe/cytology , Frontal Lobe/physiology , Models, Neurological , Physical Stimulation/methods , Somatosensory Cortex/cytologyABSTRACT
The ability of cortical networks to integrate information from different sources is essential for cognitive processes. On one hand, sensory areas exhibit fast dynamics often phase-locked to stimulation; on the other hand, frontal lobe areas with slow response latencies to stimuli must integrate and maintain information for longer periods. Thus, cortical areas may require different timescales depending on their functional role. Studying the cortical somatosensory network while monkeys discriminated between two vibrotactile stimulus patterns, we found that a hierarchical order could be established across cortical areas based on their intrinsic timescales. Further, even though subareas (areas 3b, 1, and 2) of the primary somatosensory (S1) cortex exhibit analogous firing rate responses, a clear differentiation was observed in their timescales. Importantly, we observed that this inherent timescale hierarchy was invariant between task contexts (demanding vs. nondemanding). Even if task context severely affected neural coding in cortical areas downstream to S1, their timescales remained unaffected. Moreover, we found that these time constants were invariant across neurons with different latencies or coding. Although neurons had completely different dynamics, they all exhibited comparable timescales within each cortical area. Our results suggest that this measure is demonstrative of an inherent characteristic of each cortical area, is not a dynamical feature of individual neurons, and does not depend on task demands.
Subject(s)
Cognition/physiology , Frontal Lobe/physiology , Neurons/physiology , Somatosensory Cortex/physiology , Animals , Humans , Macaca mulatta/physiology , Physical Stimulation , Reaction Time/physiologyABSTRACT
Our decisions often depend on multiple sensory experiences separated by time delays. The brain can remember these experiences and, simultaneously, estimate the timing between events. To understand the mechanisms underlying working memory and time encoding, we analyze neural activity recorded during delays in four experiments on nonhuman primates. To disambiguate potential mechanisms, we propose two analyses, namely, decoding the passage of time from neural data and computing the cumulative dimensionality of the neural trajectory over time. Time can be decoded with high precision in tasks where timing information is relevant and with lower precision when irrelevant for performing the task. Neural trajectories are always observed to be low-dimensional. In addition, our results further constrain the mechanisms underlying time encoding as we find that the linear "ramping" component of each neuron's firing rate strongly contributes to the slow timescale variations that make decoding time possible. These constraints rule out working memory models that rely on constant, sustained activity and neural networks with high-dimensional trajectories, like reservoir networks. Instead, recurrent networks trained with backpropagation capture the time-encoding properties and the dimensionality observed in the data.
Subject(s)
Memory, Short-Term/physiology , Animals , Brain/physiology , Brain Mapping/methods , Nerve Net/physiology , Neural Networks, Computer , Neurons/physiology , PrimatesABSTRACT
Several thousand years ago, our human ancestors realized that the brain was the organ of the mind and movement. But, how does the brain generate a voluntary movement and adds consciousness to it? Here, we assume that these two processes can be explained by neuroscience, but a large proportion of our society -including some scientists- considers consciousness as some immaterial substance that dwells in our body. As consequence of these divided opinions, several theories have recently emerged with the aim of explaining consciousness. These theories in no order of importance, but definitely in the order of complexity, are the global workspace (GWT), attention schema (AST), higher order-thought (HOT) and illusionist (IT) theories. All these theories originate from different backgrounds, and each tries to explain different components of consciousness: from a pure neurobiological (GWT) interpretation to a pure psychological-folk interpretation (IT).
Subject(s)
Consciousness , Neurosciences , Attention , Brain , HumansABSTRACT
Many brain areas modulate their activity during vibrotactile tasks. The activity from these areas may code the stimulus parameters, stimulus perception, or perceptual reports. Here, we discuss findings obtained in behaving monkeys aimed to understand these processes. In brief, neurons from the somatosensory thalamus and primary somatosensory cortex (S1) only code the stimulus parameters during the stimulation periods. In contrast, areas downstream of S1 code the stimulus parameters during not only the task components but also perception. Surprisingly, the midbrain dopamine system is an actor not considered before in perception. We discuss the evidence that it codes the subjective magnitude of a sensory percept. The findings reviewed here may help us to understand where and how sensation transforms into perception in the brain.
Subject(s)
Dopaminergic Neurons/physiology , Mesencephalon/physiology , Somatosensory Cortex/physiology , Thalamus/physiology , Touch Perception/physiology , Touch/physiology , AnimalsABSTRACT
Neuronal populations respond within a small number of relevant dimensions. New research by Trautmann et al. (2019) shows that spike sorting is not necessary to extract the important features of this low-dimensional population signal. Combined responses of multiple neurons (multiunit activity) only generate small changes in the extracted signals.
Subject(s)
Algorithms , Signal Processing, Computer-Assisted , Action Potentials , Neurons , Population DynamicsABSTRACT
During discrimination between two sequential vibrotactile stimulus patterns, the primate dorsal premotor cortex (DPC) neurons exhibit a complex repertoire of coding dynamics associated with the working memory, comparison, and decision components of this task. In addition, these neurons and neurons with no coding responses show complex strong fluctuations in their firing rate associated with the temporal sequence of task events. Here, to make sense of this temporal complexity, we extracted the temporal signals that were latent in the population. We found a strong link between the individual and population response, suggesting a common neural substrate. Notably, in contrast to coding dynamics, these time-dependent responses were unaffected during error trials. However, in a nondemanding task in which monkeys did not require discrimination for reward, these time-dependent signals were largely reduced and changed. These results suggest that temporal dynamics in DPC reflect the underlying cognitive processes of this task.
Subject(s)
Cognition/physiology , Memory, Short-Term/physiology , Motor Cortex/physiology , Animals , Macaca mulatta , Motor Cortex/cytologyABSTRACT
The direction of functional information flow in the sensory thalamocortical circuit may play a role in stimulus perception, but, surprisingly, this process is poorly understood. We addressed this problem by evaluating a directional information measure between simultaneously recorded neurons from somatosensory thalamus (ventral posterolateral nucleus, VPL) and somatosensory cortex (S1) sharing the same cutaneous receptive field while monkeys judged the presence or absence of a tactile stimulus. During stimulus presence, feed-forward information (VPL â S1) increased as a function of the stimulus amplitude, while pure feed-back information (S1 â VPL) was unaffected. In parallel, zero-lag interaction emerged with increasing stimulus amplitude, reflecting externally driven thalamocortical synchronization during stimulus processing. Furthermore, VPL â S1 information decreased during error trials. Also, VPL â S1 and zero-lag interaction decreased when monkeys were not required to report the stimulus presence. These findings provide evidence that both the direction of information flow and the instant synchronization in the sensory thalamocortical circuit play a role in stimulus perception.
Subject(s)
Nerve Net/physiology , Reaction Time/physiology , Somatosensory Cortex/physiology , Touch Perception/physiology , Ventral Thalamic Nuclei/physiology , Animals , Haplorhini , Nerve Net/cytology , Somatosensory Cortex/cytology , Ventral Thalamic Nuclei/cytologyABSTRACT
A 1989 paper by Patricia Goldman-Rakic and colleagues reported that the prefrontal cortex coded the visual space during working memory. This landmark work not only offered a biological explanation for this cognitive function, but also opened up a wide field of research aimed at understanding the biological bases of various cognitive functions.
Subject(s)
Cognition/physiology , Memory, Short-Term/physiology , Prefrontal Cortex/physiology , Visual Perception/physiology , Animals , Brain Mapping , Humans , Space Perception/physiologyABSTRACT
When trained monkeys discriminate the temporal structure of two sequential vibrotactile stimuli, dorsal premotor cortex (DPC) showed high heterogeneity among its neuronal responses. Notably, DPC neurons coded stimulus patterns as broader categories and signaled them during working memory, comparison, and postponed decision periods. Here, we show that such population activity can be condensed into two major coding components: one that persistently represented in working memory both the first stimulus identity and the postponed informed choice and another that transiently coded the initial sensory information and the result of the comparison between the two stimuli. Additionally, we identified relevant signals that coded the timing of task events. These temporal and task-parameter readouts were shown to be strongly linked to the monkeys' behavior when contrasted to those obtained in a non-demanding cognitive control task and during error trials. These signals, hidden in the heterogeneity, were prominently represented by the DPC population response.
Subject(s)
Action Potentials/physiology , Brain Mapping , Decision Making/physiology , Motor Cortex/cytology , Neurons/physiology , Animals , Macaca mulatta , Male , Principal Component Analysis , Psychomotor Performance , Time FactorsABSTRACT
Previous work on perceptual decision making in the sensorimotor system has shown population dynamics in the beta band, corresponding to the encoding of stimulus properties and the final decision outcome. Here, we asked how oscillatory dynamics in the medial premotor cortex (MPC) contribute to supramodal perceptual decision making. We recorded local field potentials (LFPs) and spikes in two monkeys trained to perform a tactile-acoustic frequency discrimination task, including both unimodal and crossmodal conditions. We studied the role of oscillatory activity as a function of stimulus properties (frequency and sensory modality), as well as decision outcome. We found that beta-band power correlated with relevant stimulus properties: there was a significant modulation by stimulus frequency during the working-memory (WM) retention interval, as well as modulation by stimulus modality-the latter was observed only in the case of a purely unimodal task, where modality information was relevant to prepare for the upcoming second stimulus. Furthermore, we found a significant modulation of beta power during the comparison and decision period, which was predictive of decision outcome. Finally, beta-band spike-field coherence (SFC) matched these LFP observations. In conclusion, we demonstrate that beta power in MPC is reflective of stimulus features in a supramodal, context-dependent manner, and additionally reflects the decision outcome. We propose that these beta modulations are a signature of the recruitment of functional neuronal ensembles, which encode task-relevant information.
Subject(s)
Beta Rhythm/physiology , Judgment/physiology , Memory, Short-Term/physiology , Motor Cortex/physiology , Animals , Macaca mulattaABSTRACT
Learning to associate unambiguous sensory cues with rewarded choices is known to be mediated by dopamine (DA) neurons. However, little is known about how these neurons behave when choices rely on uncertain reward-predicting stimuli. To study this issue we reanalyzed DA recordings from monkeys engaged in the detection of weak tactile stimuli delivered at random times and formulated a reinforcement learning model based on belief states. Specifically, we investigated how the firing activity of DA neurons should behave if they were coding the error in the prediction of the total future reward when animals made decisions relying on uncertain sensory and temporal information. Our results show that the same signal that codes for reward prediction errors also codes the animal's certainty about the presence of the stimulus and the temporal expectation of sensory cues.
Subject(s)
Choice Behavior/physiology , Decision Making/physiology , Dopaminergic Neurons/physiology , Haplorhini/physiology , Models, Neurological , Reward , Animals , Bayes Theorem , Cues , Dopamine/metabolism , Membrane Potentials/physiology , Mesencephalon/cytology , Mesencephalon/physiology , Microelectrodes , TouchABSTRACT
Working memory (WM) is a cognitive function for temporary maintenance and manipulation of information, which requires conversion of stimulus-driven signals into internal representations that are maintained across seconds-long mnemonic delays. Within primate prefrontal cortex (PFC), a critical node of the brain's WM network, neurons show stimulus-selective persistent activity during WM, but many of them exhibit strong temporal dynamics and heterogeneity, raising the questions of whether, and how, neuronal populations in PFC maintain stable mnemonic representations of stimuli during WM. Here we show that despite complex and heterogeneous temporal dynamics in single-neuron activity, PFC activity is endowed with a population-level coding of the mnemonic stimulus that is stable and robust throughout WM maintenance. We applied population-level analyses to hundreds of recorded single neurons from lateral PFC of monkeys performing two seminal tasks that demand parametric WM: oculomotor delayed response and vibrotactile delayed discrimination. We found that the high-dimensional state space of PFC population activity contains a low-dimensional subspace in which stimulus representations are stable across time during the cue and delay epochs, enabling robust and generalizable decoding compared with time-optimized subspaces. To explore potential mechanisms, we applied these same population-level analyses to theoretical neural circuit models of WM activity. Three previously proposed models failed to capture the key population-level features observed empirically. We propose network connectivity properties, implemented in a linear network model, which can underlie these features. This work uncovers stable population-level WM representations in PFC, despite strong temporal neural dynamics, thereby providing insights into neural circuit mechanisms supporting WM.
Subject(s)
Memory, Short-Term/physiology , Neurons/physiology , Prefrontal Cortex/physiology , Animals , Cognition/physiology , Macaca mulatta/physiology , Models, Neurological , Population DynamicsABSTRACT
The problem of neural coding in perceptual decision making revolves around two fundamental questions: (i) How are the neural representations of sensory stimuli related to perception, and (ii) what attributes of these neural responses are relevant for downstream networks, and how do they influence decision making? We studied these two questions by recording neurons in primary somatosensory (S1) and dorsal premotor (DPC) cortex while trained monkeys reported whether the temporal pattern structure of two sequential vibrotactile stimuli (of equal mean frequency) was the same or different. We found that S1 neurons coded the temporal patterns in a literal way and only during the stimulation periods and did not reflect the monkeys' decisions. In contrast, DPC neurons coded the stimulus patterns as broader categories and signaled them during the working memory, comparison, and decision periods. These results show that the initial sensory representation is transformed into an intermediate, more abstract categorical code that combines past and present information to ultimately generate a perceptually informed choice.
Subject(s)
Decision Making/physiology , Discrimination, Psychological/physiology , Motor Cortex/physiology , Pattern Recognition, Physiological , Somatosensory Cortex/physiology , Animals , Judgment , Macaca mulatta , Memory/physiology , Reaction Time , Single-Cell AnalysisABSTRACT
Neurons in higher cortical areas, such as the prefrontal cortex, are often tuned to a variety of sensory and motor variables, and are therefore said to display mixed selectivity. This complexity of single neuron responses can obscure what information these areas represent and how it is represented. Here we demonstrate the advantages of a new dimensionality reduction technique, demixed principal component analysis (dPCA), that decomposes population activity into a few components. In addition to systematically capturing the majority of the variance of the data, dPCA also exposes the dependence of the neural representation on task parameters such as stimuli, decisions, or rewards. To illustrate our method we reanalyze population data from four datasets comprising different species, different cortical areas and different experimental tasks. In each case, dPCA provides a concise way of visualizing the data that summarizes the task-dependent features of the population response in a single figure.