Non-additive activity modulation during a decision making task involving tactic selection

Abstract

Human brain imaging has revealed that stimulus-induced activity does generally not simply add to the pre-stimulus activity, but rather builds in a non-additive way on this activity. Here we investigate this subject at the single neuron level and address the question whether and to what extent a strong form of non-additivity where activity drops post-cue is present in different areas of monkey cortex, including prefrontal and agranular frontal areas, during a perceptual decision making task involving action and tactic selection. Specifically we analyze spike train data recorded in vivo from the posterior dorsomedial prefrontal cortex (pmPFC), the supplementary motor area (SMA) and the presupplementary motor area (pre-SMA). For each neuron, we compute the ratio of the trial-averaged pre-stimulus spike count to the trial-averaged post-stimulus count. We also perform the ratio and averaging procedures in reverse order. We find that the statistics of these quantities behave differently across areas. pmPFC involved in tactic selection shows stronger non-additivity compared to the two other areas which more generically just increase their firing rate pos-stimulus. pmPFC behaved more similarly to pre-SMA, a likely consequence of the reciprocal connections between these areas. The trial-averaged ratio statistic was reproduced by a surrogate inhomogeneous Poisson process in which the measured trial-averaged firing rate for a given neuron is used as its time-dependent rate. Principal component analysis (PCA) of the trial-averaged firing rates of neuronal ensembles further reveals area-specific time courses of response to the stimulus, including latency to peak neural response, for the typical population activity. Our work demonstrates subtle forms of area-specific non-additivity based on the fine variability structure of pre- and post-stimulus spiking activity on the single neuron level. It also reveals significant differences between areas for PCA and surrogate analysis, complementing previous observations of regional differences based solely on post-stimulus responses. Moreover, we observe regional differences in non-additivity which are related to the monkey’s successful tactic selection and decision making.

From Shorter to Longer Timescales: Converging Integrated Information Theory (IIT) with the Temporo-Spatial Theory of Consciousness (TTC)

“…Such a non-additive pre-stimulus-stimulus interaction is indeed confirmed by recent studies in fMRI [ 52 ], EEG/MEG [ 53 , 55 , 83 , 84 ], and cellular recordings [ 85 ]. The pre-stimulus activity provides a temporo-spatial context by means of which it can strongly shape the activity that the external input or stimulus can (or cannot) elicit, that is, stimulus-induced activity: the input effects are not simply added to the ongoing activity ( Figure 2 ).…”

“…How can we measure the impact of pre-stimulus activity during post-stimulus activity? One way is to measure trial-to-trial variability (TTV) that can be observed at both the levels of cellular and regional-systemic activity [ 78 , 85 , 86 , 87 , 88 ]. TTV measures the variation in the amplitude across different trials of one and the same stimulus.…”

“…Furthermore, recent studies in EEG/MEG [ 53 , 54 , 55 , 84 ] and on the cellular level [ 85 ] demonstrate that the level of post-stimulus TTV is strongly dependent on pre-stimulus activity. High levels of pre-stimulus activity lead to higher degrees of transient post-stimulus suppression than low levels of pre-stimulus activity.…”

Interacting ventral temporal gradients of timescales and functional connectivity and their relationships to visual behavior

“… 7 , 52 Rather, these results suggest that the anatomical differences in these types of timescales are governed by different combinations of factors that can depend on cognitive and neural context. 53 That said, there is increasing evidence that prestimulus activity can influence poststimulus activity on a trial-by-trial basis, 54 , 55 , 56 including a prior study from our group using a subset of the data presented here. 55 The results here do not contradict these prior observations, as this study examines anatomical differences in mean dynamics, not trial-by-trial relationships.…”