Neural basis for categorical boundaries in the primate pre-SMA during relative categorization of time intervals

Abstract

Perceptual categorization depends on the assignment of different stimuli to specific groups based, in principle, on the notion of flexible categorical boundaries. To determine the neural basis of categorical boundaries, we record the activity of pre-SMA neurons of monkeys executing an interval categorization task in which the limit between short and long categories changes between blocks of trials within a session. A large population of cells encodes this boundary by reaching a constant peak of activity close to the corresponding subjective limit. Notably, the time at which this peak is reached changes according to the categorical boundary of the current block, predicting the monkeys’ categorical decision on a trial-by-trial basis. In addition, pre-SMA cells also represent the category selected by the monkeys and the outcome of the decision. These results suggest that the pre-SMA adaptively encodes subjective duration boundaries between short and long durations and contains crucial neural information to categorize intervals and evaluate the outcome of such perceptual decisions.

Perturbation of Macaque Supplementary Motor Area Produces Context-Independent Changes in the Probability of Movement Initiation

“…Thus, both stimulation and recording results (Romo and Schultz, 1987;Kurata and Wise, 1988;Thaler et al, 1988;Picard and Strick, 2003;Hayduk-Costa et al, 2013;Carlsen et al, 2015;Lara et al, 2018b) argue that SMA contributes to initiation across a broad range of situations. However, the context independence of stimulation effects might appear to conflict with the well-established dependence of SMA neural responses on contextual factors (Tanji and Shima, 1994;Nakamura et al, 1998;Merchant and Georgopoulos, 2006;Merchant et al, 2011Merchant et al, , 2013Nakajima et al, 2013;Merchant and Averbeck, 2017;Lara et al, 2018b;Mendoza et al, 2018;Wang et al, 2018). Indeed, we have confirmed strongly context-dependent responses in SMA (but not motor cortex) in this very same task, at recording sites interspersed among the stimulation sites (Lara et al, 2018b).…”

“…Stimulation may disrupt motor preparation, as occurs in premotor cortex (Churchland and Shenoy, 2007). Stimulation may alter computations related to interval timing (Mita et al, 2009;Merchant et al, 2013;Merchant and de Lafuente, 2014;Cadena-Valencia et al, 2018) or time discrimination (Mendoza et al, 2018). Producing appropriately timed movements, in different ways for the different contexts, is a key aspect of our task.…”

Movement Improves the Quality of Temporal Perception and Decision Making

“…With respect to the potential neural mediators of the effects in our study, we note that recent evidence suggests that neurons within the supplementary motor area (SMA) code for subjective duration (Mita et al, 2009), and EEG activity putatively driven by the SMA has been shown to vary on a trial-by-trial basis with duration categorization (Wiener and Thompson, 2015). Further evidence has recently revealed that SMA neurons encode a categorical boundary for classifying intervals (Mendoza et al, 2018). Yet, alternative explanations suggest this region more broadly encodes response caution, and the evaluation of evidence in favor of a decision (van et al, 2011).…”

Multiplexing of EEG signatures for temporal and spatial distance estimates

“…One possibility here is that frontal beta oscillations underlie proximity to a memory standard used for judging relative duration (Wiener, et al 2018;Mendoza, et al 2018), whereas posterior alpha oscillations underlie the encoding of spatial distances in memory (Khader, et al 2010;Sauseng, et al 2005;Sutterer, et al 2019). Notably, in an fMRI version of the distance reproduction task used here, greater hippocampal activation was observed as subjects completed distance reproductions, which further correlated with the degree of central tendency between subjects (Wiener, et al 2016).…”