Behavioural and neuronal correlates of sensory prioritization in the rat whisker system

Abstract

Animals need to assess when to initiate actions based on uncertain sensory evidence. To formulate a response, decision making systems must prioritize extraction of neuronal signals that represent ecologically relevant events from signals that are behaviorally less relevant. This is commonly known as selective attention. The current thesis aims to investigate two simple forms of attention in rodents: sensory prioritization to a specific modality and temporal cueing. The rat whisker system is functionally efficient, and anatomically well characterized. We therefore utilize the whisker touch as a model sensory system to investigate the neuronal and behavioral correlates of attention in rats.

We begin this thesis by designing a novel simple detection task that investigated whether rats dedicate attentional resources to the sensory modality in which a near-threshold event is more likely to occur. Detection of low-amplitude events is critical to survival, and to formulate a response, animals must extract minute neuronal signals from the sensory modality that is more likely to provide key information. We manipulated attention by controlling the likelihood with which a stimulus was presented from one of two modalities. In a whisker session, 80% of trials contained a brief vibration stimulus applied to whiskers and the remaining 20% of trials contained a brief change of luminance. These likelihoods were reversed in a visual session. When a stimulus was presented in the high-likelihood context, detection performance increased and was faster compared with the same stimulus presented in the low-likelihood context. Sensory prioritization was also reflected in neuronal activity in the vibrissal area of primary somatosensory cortex: single units responded differentially to a whisker vibration stimulus when presented with higher probability compared to the same stimulus when presented with lower probability. Neuronal activity in the vibrissal cortex displayed signatures of multiplicative gain control and enhanced response to vibration stimuli during the whisker session. In Chapter 3, we replicated these findings in a forced choice paradigm and extended the investigation from somatosensory/visual to the somatosensory/auditory. Attention was similarly manipulated by controlling likelihoods of stimulus presentation. Again, we observed improvements in detection performance and reaction time, as well as improvements in discrimination performance for stimuli presented in a high-likelihood context. The behavioral consequences of a forced choice compared to simple detection task are discussed.

Finally, we developed a novel task that investigated whether rats were able to dedicate attentional resources in time. Operating with some finite quantity of attentional resources, by direct these resources at the expected time, animals would benefit from prioritizing processing based on temporal cues. We manipulated temporal cueing by presenting an auditory cue that preceded a target vibration stimulus in a subset of trials. On another subset, no auditory cue was presented. Presentations of these trials were of equal probability. Critically in this paradigm, the auditory cue provided temporal information but did not provide any spatial information about the location of the vibration stimulus. The auditory cue increased detection and discrimination performances and resulted in faster responses compared to trials in which the cue was absent. We observed neuronal signatures of temporal cuing in the vibrissal area of the primary somatosensory cortex. Single units showed enhanced response to the vibration stimulus during trials in which the stimulus was temporally expected. However, we did not observe signatures of multiplicative gain control in this paradigm. Instead, a decrease in baseline activity was observed that was phase locked to the onset of the auditory cue.

In summary, this thesis presents two novel paradigms to study selective attention in rats in the form of sensory prioritization and temporal cueing. In addition, we investigate the neuronal correlates of selective attention in the vibrissal area of the primary somatosensory cortex. These series of experiments establish the rat as an alternative model organism to primates for studying attention.