RESUMEN
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.
Asunto(s)
Macaca mulatta , Corteza Somatosensorial , Animales , Corteza Somatosensorial/fisiología , Modelos Neurológicos , MasculinoRESUMEN
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.
Asunto(s)
Corteza Somatosensorial , Percepción del Tacto , Animales , Corteza Somatosensorial/fisiología , Percepción del Tacto/fisiología , Tacto , Lóbulo Parietal , Células Receptoras SensorialesRESUMEN
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.
Asunto(s)
Corteza Motora , Corteza Motora/fisiología , Neuronas/fisiología , Movimiento/fisiologíaRESUMEN
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.
Asunto(s)
Macaca mulatta/fisiología , Neuronas/fisiología , Células Receptoras Sensoriales/fisiología , Corteza Somatosensorial/fisiología , Percepción del Tacto/fisiología , Algoritmos , Animales , Lóbulo Frontal/citología , Lóbulo Frontal/fisiología , Modelos Neurológicos , Estimulación Física/métodos , Corteza Somatosensorial/citologíaRESUMEN
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.
Asunto(s)
Toma de Decisiones/fisiología , Discriminación en Psicología/fisiología , Corteza Motora/fisiología , Patrones de Reconocimiento Fisiológico , Corteza Somatosensorial/fisiología , Animales , Juicio , Macaca mulatta , Memoria/fisiología , Tiempo de Reacción , Análisis de la Célula IndividualRESUMEN
The contribution of the sensory thalamus to perception and decision making is not well understood. We addressed this problem by recording single neurons in the ventral posterior lateral (VPL) nucleus of the somatosensory thalamus while trained monkeys judged the presence or absence of a vibrotactile stimulus of variable amplitude applied to the skin of a fingertip. We found that neurons in the VPL nucleus modulated their firing rate as a function of stimulus amplitude, and that such modulations accounted for the monkeys' overall psychophysical performance. These neural responses did not predict the animals' decision reports in individual trials, however. Moreover, the sensitivity to changes in stimulus amplitude was similar when the monkeys' performed the detection task and when they were not required to report stimulus detection. These results suggest that the primate somatosensory thalamus likely provides a reliable neural representation of the sensory input to the cerebral cortex, where sensory information is transformed and combined with other cognitive components associated with behavioral performance.
Asunto(s)
Toma de Decisiones/fisiología , Tálamo/fisiología , Percepción del Tacto/fisiología , Núcleos Talámicos Ventrales/citología , Animales , Macaca mulatta , Microelectrodos , Neuronas , Estimulación Física , Desempeño Psicomotor , Psicofísica , Curva ROCRESUMEN
Recent studies have reported that sensory cortices process more than one sensory modality, challenging the long-lasting concept that they process only one. However, both the identity of these multimodal responses and whether they contribute to perceptual judgments is unclear. We recorded from single neurons in somatosensory cortices and primary auditory cortex while trained monkeys discriminated, on interleaved trials, either between two tactile flutter stimuli or between two acoustic flutter stimuli, and during discrimination sets that combined these two sensory modalities. We found neurons in these sensory cortices that responded to stimuli that are not of their principal sensory modality during these tasks. However, the identity of the stimulus could only be decoded from responses to their principal sensory modality during the stimulation periods and not during the processing steps that link sensation and decision making. These results suggest that multimodal encoding and perceptual judgments in these tasks occur outside the sensory cortices studied here.
Asunto(s)
Corteza Auditiva/fisiología , Percepción Auditiva/fisiología , Discriminación en Psicología/fisiología , Juicio/fisiología , Células Receptoras Sensoriales/fisiología , Percepción del Tacto/fisiología , Estimulación Acústica/métodos , Potenciales de Acción/fisiología , Animales , Corteza Auditiva/citología , Mapeo Encefálico , Toma de Decisiones/fisiología , Macaca mulatta , Psicoacústica , Corteza Somatosensorial/citología , Tacto/fisiologíaRESUMEN
Perceptual decisions arise from the activity of neurons distributed across brain circuits. But, decoding the mechanisms behind this cognitive operation across brain circuits has long posed a difficult problem. We recorded the neuronal activity of diverse cortical areas, while monkeys performed a vibrotactile discrimination task. We find that the encoding of the stimuli during the stimulus periods, working memory, and comparison periods is widely distributed across cortical areas. Notably, during the comparison and postponed decision report periods the activity of frontal brain circuits encode both the result of the sensory evaluation that corresponds to the monkey's possible choices and past information on which the decision is based. These results suggest that frontal lobe circuits are more engaged in the readout of sensory information from working memory, when it is required to be compared with other sensory inputs, than simply engaged in motor responses during this task.
Asunto(s)
Corteza Cerebral/fisiología , Conducta de Elección/fisiología , Aprendizaje Discriminativo/fisiología , Neuronas/fisiología , Animales , Mapeo Encefálico , Electrofisiología , Macaca mulatta , Red Nerviosa/fisiología , Pruebas Neuropsicológicas , Estimulación Física , Desempeño Psicomotor/fisiología , VibraciónRESUMEN
We report a procedure for recording the simultaneous activity of single neurons distributed across five cortical areas in behaving monkeys. The procedure consists of a commercially available microdrive adapted to a commercially available neural data collection system. The critical advantage of this procedure is that, in each cortical area, a configuration of seven microelectrodes spaced 250-500 mum can be inserted transdurally and each can be moved independently in the z axis. For each microelectrode, the data collection system can record the activity of up to five neurons together with the local field potential (LFP). With this procedure, we normally monitor the simultaneous activity of 70-100 neurons while trained monkeys discriminate the difference in frequency between two vibrotactile stimuli. Approximately 20-60 of these neurons have response properties previously reported in this task. The neuronal recordings show good signal-to-noise ratio, are remarkably stable along a 1-day session, and allow testing several protocols. Microelectrodes are removed from the brain after a 1-day recording session, but are reinserted again the next day by using the same or different x-y microelectrode array configurations. The fact that microelectrodes can be moved in the z axis during the recording session and that the x-y configuration can be changed from day to day maximizes the probability of studying simultaneous interactions, both local and across distant cortical areas, between neurons associated with the different components of this task.
Asunto(s)
Corteza Cerebral/fisiología , Neuronas/fisiología , Percepción/fisiología , Potenciales de Acción , Animales , Mapeo Encefálico , Electrofisiología , Haplorrinos , Métodos , Microelectrodos , Estimulación FísicaRESUMEN
During a sensory discrimination task, the responses of multiple sensory neurons must be combined to generate a choice. The optimal combination of responses is determined both by their dependence on the sensory stimulus and by their cofluctuations across trials-that is, the noise correlations. Positively correlated noise is considered deleterious, because it limits the coding accuracy of populations of similarly tuned neurons. However, positively correlated fluctuations between differently tuned neurons actually increase coding accuracy, because they allow the common noise to be subtracted without signal loss. This is demonstrated with data recorded from the secondary somatosensory cortex of monkeys performing a vibrotactile discrimination task. The results indicate that positive correlations are not always harmful and may be exploited by cortical networks to enhance the neural representation of features to be discriminated.
Asunto(s)
Aprendizaje Discriminativo/fisiología , Modelos Neurológicos , Neuronas/fisiología , Corteza Somatosensorial/fisiología , Tacto/fisiología , Animales , Electrofisiología , Modelos Lineales , Macaca mulatta , Psicofísica , Corteza Somatosensorial/citología , VibraciónRESUMEN
Key to understanding somatosensation is the form of how the mechanical stimuli are represented in the evoked neuronal activity of the brain. Here, we focus on studies that address the question of which components of the evoked neuronal activity in the somatosensory system represent the stimulus features. We review experiments that probe whether these neuronal representations are essential to somatosensation. We also discuss recent results that suggest how the somatosensory stimuli are represented in the brain during short-term memory. Finally, we review data that show the neuronal correlates of a decision during somatosensory perception.
Asunto(s)
Conducta/fisiología , Encéfalo/fisiología , Sensación/fisiología , Animales , Discriminación en Psicología/fisiología , Haplorrinos , Humanos , Neuronas Aferentes/fisiología , Estimulación Física , Psicofísica , Corteza Somatosensorial/fisiología , VibraciónRESUMEN
The events linking sensory discrimination to motor action remain unclear. It is not known, for example, whether the motor areas of the frontal lobe receive the result of the discrimination process from other areas or whether they actively participate in it. To investigate this, we trained monkeys to discriminate between two mechanical vibrations applied sequentially to the fingertips; here subjects had to recall the first vibration, compare it to the second one, and indicate with a hand/arm movement which of the two vibrations had the higher frequency. We recorded the activity of single neurons in medial premotor cortex (MPC) and found that their responses correlate with the diverse stages of the discrimination process. Thus, activity in MPC reflects the temporal evolution of the decision-making process leading to action selection during this perceptual task.