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.behaving monkeys | somatosensory cortex | dorsal premotor cortex | pattern discrimination | categorical code F rom the most stereotyped behavior of invertebrates to the most elaborate behavior of primates, a central issue in neurobiology is elucidating how sensory information is represented in neural circuits and how it is used to generate actions. In principle, this process can be understood as a chain of three basic neuronal operations. The representation of the physical/chemical attributes of the environment and the execution of motor commands can be regarded as the end points of this chain of neuronal operations. In the middle of this chain is a crucial processing step in which the sensory representations are analyzed and transformed in such a manner that the nervous system is able to choose the adequate motor action.We have investigated this chain of processes by analyzing the neuronal activity of parietal and frontal cortices in trained monkeys performing a vibrotactile frequency discrimination task (VFDT; reviewed in refs. 1-3). In this task, monkeys compared the frequencies of two vibratory stimuli applied sequentially to the skin of one fingertip and then used their free hand to push one of two response buttons to indicate whether the second stimulus frequency (f2) was lower or higher than the first stimulus frequency (f1). The VFDT, although apparently simple, is designed so that it can only be executed when a minimum number of neuronal operations or cognitive steps are performed: coding f1, holding f1 in working memory, comparing f2 with the memory trace of f1, and, finally, executing a motor response to indicate whether f2 > f1 or f2 < f1. Thus, the VFDT allowed us to investigate a wide range of essential neural processes during perceptual decision making (1-3). However, the VFDT poses a fundamental problem: What is the neural code(s) that an observer might use to decide whether f2 > f1 or f2 < f1?...

Working memory, a well-studied cognitive function, refers to the capacity to remember things for a short time. Which neurons in the brain implement this function and how exactly they do it are unresolved questions. Here we show that, in a cortical area that participates in the analysis of perceptual experiences, the same neurons encode both tactile and acoustic information in working memory, and do so using the same representation for both modalities. This means that memory circuits in this area are dedicated to encoding information in a relatively abstract format that had not been revealed until now.

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.

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.behaving monkeys | dorsal premotor cortex | temporal signals | contextdependent signals | ramping activity O ur ability to anticipate the occurrence of future events is crucial when performing many cognitively demanding behaviors. For example, the benefits of anticipating the arrival of sensory inputs can be decisive in our perceptual behavior (1-3). In this way, neural circuits engaged in cognitive processes of this type would profit from employing temporal signals. Thus, the timing information contained in those signals may then constitute a mechanism to anticipate future task events. In fact, during experiments it is common to find neurons that display noteworthy temporal dependencies in their firing rate (4-9). In particular, a large proportion of the individual neurons from the frontal lobe cortices exhibit intricate time-dependent responses that mesh in myriad ways with stimulus identity and decision outcomes during behavioral tasks (4, 10-12). However, individual neurons must be reflecting a more widespread response across the network; temporal signals that represent anticipation of task events and stimulus identity must be coded at the population level. Recently, these neuronal population signals from the frontal lobe cortex were studied employing methods that reduced the dimensionality of network dynamics (11,13). These methodological approaches facilitated the recognition of latent population responses during cognitive tasks (14-17). Notably, large differences between the population variance related to purely temporal signals and task parameter coding were observed (11,13). Markedly, even if the tasks examined were completely different and employed two types of animal models, the temporal signals always captured more than 65% of the total variance. These results indicate that temporal signals occupy a central role during the execution of any behavioral task.Here, to further investigate the temporal responses in single units and neuronal population, we employed the network activity recorded i...

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.