Repetition suppression for visual actions in the macaque superior temporal sulcus

Abstract

In many brain areas, repetition of a stimulus usually weakens the neural response. This "adaptation" or repetition suppression effect has been observed with mass potential measures such as event-related potentials (ERPs), in fMRI BOLD responses, and locally with local field potentials (LFPs) and spiking activity. Recently, it has been reported that macaque F5 mirror neurons do not show repetition suppression of their spiking activity for single repetitions of hand actions, which disagrees with human fMRI adaptation studies. This finding also contrasts with numerous studies showing repetition suppression in macaque inferior temporal cortex, including the rostral superior temporal sulcus (STS). Since the latter studies employed static stimuli, we assessed here whether the use of dynamic action stimuli abolishes repetition suppression in the awake macaque STS. To assess adaptation effects in the STS, we employed the same hand action movies as used when examining adaptation in F5. The upper bank STS neurons showed repetition suppression during the approaching phase of the hand action, which corresponded to the phase of the action for which these neurons responded overall the strongest. The repetition suppression was present for the spiking activity measured in independent single-unit and multiunit recordings as well as for the LFP power at frequencies > 50 Hz. Together with previous data in F5, these findings suggest that adaptation effects differ between F5 mirror neurons and the STS neurons.

Adaptation aftereffects reveal representations for encoding of contingent social actions

“…Visual action recognition has been associated with activation in superior temporal sulcus (STS) ( 28 – 30 ). Some evidence from imaging ( 31 ) and physiological ( 7 ) studies shows that visual adaptation with the action stimuli transiently changes the neural response properties in area STS. Other studies, however, show an adaptation effect in response to actions in inferior parietal lobule and inferior frontal gyrus areas ( 16 , 32 ).…”

“…Specifically, behavioral adaptation can selectively target the neural mechanisms and tuning characteristics of perceptual processes across the cortical hierarchy ( 1 – 4 ). The inference about the neural mechanisms from the behavioral adaptation is grounded in electrophysiological studies showing how repetitive sensory stimulation results in a transient response decrease in the neuronal populations involved in the processing of the stimulus ( 5 – 12 ). As a behavioral consequence of this neural mechanism, the perception of a subsequently presented ambiguous test stimulus is altered for a short period.…”

Action adaptation during natural unfolding social scenes influences action recognition and inferences made about actor beliefs

“…That adaptation to one action does not transfer to a different action indicates that adaptation is not acting at an action-independent abstract level but rather at an action-dependent level. Rather, we believe that adaptation at a conceptually lower level where the actions themselves are distinguished (Barraclough & Jellema, 2011;Kuravi, Caggiano, Giese, & Vogels, 2016) is the most parsimonious explanation for the effects we observed in Experiment 5. Adaptation to the adapting actor underestimating the weight of the box will also result in adaptation to kinematics associated with lifting an unexpectedly heavier box.…”

“…Visual adaptation to hand actions ) and whole-body actions (Barraclough & Jellema, 2011) influences the subsequent recognition of hand and whole-body actions, respectively. These effects are likely to be due to the selective adaptation of single neurons within the STS that are responsive to specific actions (Kuravi, Caggiano, Giese, & Vogels, 2016). Although adaptation paradigms have been used to demonstrate that action aftereffects can be modulated by social context (de la Rosa et al, 2014), these effects are probably due to a top-down modulation of action recognition mechanisms.…”

Visual adaptation enhances action sound discrimination

“…Neurons within the STS of the monkey respond selectively to the hand actions of other individuals (Chitty, Perrett, Mistlin, & Potter, 1985a, 1985b; Perrett et al, 1989), and many of them integrate the specific visual and auditory information about the action itself (Barraclough et al, 2005). Furthermore, the population of cells within the STS appear to represent actions contiguously across a parametric action space (Barraclough et al, 2009; Vangeneugden, Pollick, & Vogels, 2009), while action-sensitive cells in the STS are also susceptible to adaptation (Kuravi, Caggiano, Giese, & Vogels, 2016). Thus, adaptation-induced changes in activity within a population of neurons of these types may underlie the two effects we observe in this study.…”