The influence of saccadic eye movements on neural activity in the temporal lobe

The responses of cells in the temporal lobe to faces and objects has been the topic of extensive research; however, the eye movement constraints during these experiments varies considerably. Some require central eye fixation during image presentation, whereas others allow unconstrained viewing of stimuli. Here, we explore the influence of saccadic eye movements on neural responses in the temporal lobe. Awake macaques were presented with a set of objects or faces while we recorded simultaneously from neurons in the upper-bank of the superior temporal sulcus (STS) and in the auditory cortex. Responses during three categories of saccades were evaluated: 1) those occurring prior to fixation onset (spontaneous saccades), 2) those made at the time of central cue fixation (visually-guided saccades) and 3) saccades made during scanning of an image (image-guided saccades). Saccade modulation was observed for all categories of saccades, though not always in the same cells, and irrespective of a cell’s image selectivity. Single unit responses typically occurred during negative components of the local field potential (LFP). Whereas broad peri-saccadic modulation was seen in both STS and auditory cortex, only cells in STS showed precise, short-latency responses at the termination of a saccade. The results of our study demonstrate that even those cells that respond to face and object stimuli can show modulation to eye movements. In addition, saccade modulation is not limited to classically-defined image-responsive regions of the brain: broad peri-saccadic modulation was also observed in auditory cortex. The observation that actions can influence sensory responses will be considered within the framework of embodied cognition

Beyond the Simple "Face Cell": Response Modulation of Neurons in the Superior Temporal Sulcus to Saccadic Eye Movements

Human and non-human primates have evolved specialized abilities to distinguish among conspecifics' facial characteristics such as identity and facial expression. A cortical network in the temporal lobe of the monkey has been implicated in such specialized perception, though it is possible that additional factors could contribute to the responses of temporal lobe neurons. Objectives: In this study, we explore the influence of eye movements on neural responses in the temporal lobe. In addition we will determine whether neurons responsive to face stimuli are also saccade-modulated, and if so, whether modulation to both can occur simultaneously, while scanning face images. Materials and Methods: Awake macaques were presented with a set of clip-art objects or faces of monkeys displaying aggressive, neutral, and appeasing expressions while we recorded from neurons in the superior temporal sulcus (STS). Evoked responses to the images were evaluated, in addition to responses to saccades occurring prior to fixation onset (spontaneous saccades), at the time of central cue fixation (visually-guided saccades) and while an image was viewed (image-guided saccades). Results: We found identity-selective as well as expression-selective unit responses to the face stimuli within the upper bank STS, as well as overall preferences for faces or objects. The unit responses were typically consistent with fluctuations in the local field potential (LFP). Both unit and LFP responses showed peri-saccadic modulation, whether for spontaneous or visually-guided saccades. In addition to describing this general saccadic modulation, we will discuss the modulation of saccadic eye movements during stimulus response window (i.e.100-500 ms after image onset). Conclusion: The results of our study not only demonstrate neuronal selectivity for facial expressions and identity in the upper bank STS but also provide evidence that such neurons are influenced by eye movements. Saccadic modulation of face-selective neurons may be understood within the framework of embodied cognition

Saccades during Object Viewing Modulate Oscillatory Phase in the Superior Temporal Sulcus

Saccadic eye movements (SEMs) are the primary means of gating visual information in primates and strongly influence visual perception. The active exploration of the visual environment (“active vision”) via SEMs produces suppression during saccades and enhancement afterward (i.e., during fixation) in occipital visual areas. In lateral temporal lobe visual areas, the influence, if any, of eye movements is less well understood, despite the necessity of these areas for forming coherent percepts of objects. The upper bank of the superior temporal sulcus (uSTS) is one such area whose sensitivity to SEMs is unknown. We therefore examined how saccades modulate local field potentials (LFPs) in the uSTS of macaque monkeys while they viewed face and nonface object stimuli. LFP phase concentration increased following fixation onset in the alpha (8–14 Hz), beta (14–30 Hz), and gamma (30–60 Hz) bands and was distinct from the image-evoked response. Furthermore, near-coincident onsets of fixation and image presentation—like those occurring in active vision—led to enhanced responses through greater phase concentration in the same frequency bands. Finally, single-unit activity was modulated by the phase of alpha, beta, and gamma oscillations, suggesting that the observed phase-locking influences spike timing in uSTS. Previous research implicates phase concentration in these frequency bands as a correlate of perceptual performance (Womelsdorf et al., 2006; Bosman et al., 2009). Together, these results demonstrate sensitivity to eye movements in an object-processing region of the brain and represent a plausible neural basis for the enhancement of object processing during active vision