Time course of allocation of spatial attention by acoustic cues in non‐human primates

Abstract

Spatial attention mediates the selection of information from different parts of space. When a brief cue is presented shortly before a target (cue to target onset asynchrony = CTOA) in the same location, behavioral responses are facilitated, a process called attention capture. At longer CTOAs responses to targets presented in the same location are inhibited, called inhibition of return (IOR). In the visual modality, these processes have been demonstrated in both humans and non-human primates, the latter allowing for the study of the underlying neural mechanisms. In audition, the effects of attention have only been shown in humans when the experimental task required sound localization. Studies in monkeys using similar cues but lacking a sound localization requirement have produced negative results.We have studied the effects of predictive acoustic cues on the latency of gaze shifts to visual and auditory targets in monkeys experienced in localizing sound sources in the laboratory with the head unrestrained. Both attention capture and IOR were demonstrated using acoustic cues though on a faster time course compared to visual cues. Additionally, the effect was observed across sensory modalities (acoustic cue to visual target) suggesting that the underlying neural mechanisms of these effects may be mediated within the superior colliculus, a center where inputs from both vision and audition converge.

Changing auditory time with prismatic goggles

“…The brain reconstructs the spatial location of an auditory stimulus based on interaural and monaural auditory cues (Blauert & Lindemann, 1986), and the output of this computation is typically less precise than the localization of a visual stimulus. Studies on animals (Lee & Middlebrooks, 2010;Populin & Rajala, 2010) and humans (Pavani, Làdavas, & Driver, 2002) have also shown that localization of sounds is most precise when the spatial encoding of the auditory stimuli is salient for the task. In cats, Lee and Middlebrooks (2010) showed that the width of spatial receptive fields (from 180°to 360°) of neurons in the auditory primary cortex (A1) becomes sharper when the localization of sounds is requested by the task, as compared to when spatial factors are not salient for the animal's behavior.…”

Neural correlate of auditory spatial attention allocation in the superior colliculus

“…Two adult male rhesus monkeys (Macaca mulatta), weighing 7.5 and 10 kg, participated in this study. One of them, subject G, had contributed to our previous behavioral report (Populin and Rajala 2010). The animals were prepared for eye movement recordings with the scleral search coil technique (Robinson 1963) by implanting coils constructed from teflon-coated stainlesssteel wire (SA632; Cooner Wire, Chatsworth, CA), using the approach described by Judge et al (1980).…”

“…Using gaze latency as the dependent variable, our data demonstrated that rhesus monkeys could indeed allocate spatial attention based on auditory spatial information. Moreover, they showed that the effects followed the classical attention capture (AC) (Jonides 1981) and inhibition of return (IOR; Posner and Cohen 1984) pattern that characterizes the allocation of spatial attention in the visual modality, albeit with a faster time course (Populin and Rajala 2010).…”

“…In a previous behavioral study, we addressed a major discrepancy between results from humans and monkeys concerning the allocation of spatial attention in the auditory modality (Populin and Rajala 2010). Specifically, it had been demonstrated that humans could allocate spatial attention about the surrounding space based on auditory signals, provided that the sources of the signals were localized, not just detected (Mc-Donald and Ward 1999;Posner 1978;Rhodes 1987;Roberts et al 2009; Spence and Driver 1994); however, rhesus monkeys, the animal model closest to humans for studies of the function of the nervous system, and specifically for the mechanisms underlying the allocation of visual attention (Bisley and Goldberg 2010;Colby and Goldberg 1999;Desimone and Duncan 1995;Reynolds and Chelazzi 2004;Squire et al 2013), could not (Bell et al 2004).…”

“…Accordingly, because we had demonstrated that auditory cues do lead to the attentional effects of AC and IOR under specific task conditions (Populin and Rajala 2010), we hypothesized that iSC neurons should exhibit similar cue-target interactions in animals that have been trained to orient to the sources of auditory stimulation with their heads unrestrained for rewards. The results from two rhesus monkeys tested with broadband auditory cues revealed that a similar correlation between behavioral manifestations of spatial attention allocation, AC and IOR, and modulation of target-evoked responses is found in iSC neurons.…”