Attentional Capture? Synchronized Feedback Signals from the Isthmi Boost Retinal Signals to Higher Visual Areas

Abstract

When a salient object in the visual field captures attention, the neural representation of that object is enhanced at the expense of competing stimuli. How neural activity evoked by a salient stimulus evolves to take precedence over the neural activity evoked by other stimuli is a matter of intensive investigation. Here, we describe in pigeons (Columba livia) how retinal inputs to the optic tectum (TeO, superior colliculus in mammals), triggered by moving stimuli, are selectively relayed on to the rotundus (Rt, caudal pulvinar) in the thalamus, and to its pallial target, the entopallium (E, extrastriate cortex). We show that two satellite nuclei of the TeO, the nucleus isthmi parvocelullaris (Ipc) and isthmi semilunaris (SLu), send synchronized feedback signals across tectal layers. Preventing the feedback from Ipc but not from SLu to a tectal location suppresses visual responses to moving stimuli from the corresponding region of visual space in all Rt subdivisions. In addition, the bursting feedback from the Ipc imprints a bursting rhythm on the visual signals, such that the visual responses of the Rt and the E acquire a bursting modulation significantly synchronized to the feedback from Ipc. As the Ipc feedback signals are selected by competitive interactions, the visual responses within the receptive fields in the Rt tend to synchronize with the tectal location receiving the "winning" feedback from Ipc. We propose that this selective transmission of afferent activity combined with the cross-regional synchronization of the areas involved represents a bottom-up mechanism by which salient stimuli capture attention.

Ongoing activity in the optic tectum is correlated on a trial-by-trial basis with the pupil dilation response

“…One main inhibition pathway to the OT originates in nucleus isthmi magnocellularis (Felix et al 1994;Luksch 2003;. This pathway was suggested to be involved in stimulus selection (Lai et al 2011;Marin et al 2012;Mysore et al 2010;Mysore and Knudsen 2013), and therefore its removal is expected to result in stronger responses to stimuli as well as greater ongoing activity. However, inhibition from nucleus isthmi magnocellularis is global, inhibiting large portions of the OT (Knudsen 2011;Wang et al 2004), and it therefore cannot explain the locality of the correlation (Fig.…”

“…Both pathways are topographic (Marin et al 2007;Wang et al 2006;Winkowski and Knudsen 2007) and can therefore account for the locality of the correlation effect. Moreover, both pathways have been linked with the process of stimulus selection Marin et al 2007Marin et al , 2012Winkowski and Knudsen 2006). Future pharmacological experiments should be able to discern between the different possibilities.…”

“…Moreover, the cross-correlograms between these two structures were dominated by gamma band oscillations (Marin et al 2012). Here we show that the level of ongoing activity in the OT and the entopallium tends to be correlated and to predict behavioral responses.…”

“…This result suggests that information about the behavioral response to a stimulus may be found in the correlations of spikes between tectal and entopallial neurons and further supports the notion that the OT and the entopallium work in concert to select and control orienting responses. (Marin et al 2007(Marin et al , 2012Gutfreund 2012).…”

“…Recent studies suggested that the power of induced gamma oscillations in the avian tectum carries information about the stimulus and is related to spatial attention (Marin et al 2012;Sridharan et al 2011). It is therefore of interest to characterize fluctuations of the ongoing LFP signal and examine its correlation with the ongoing fluctuations of the multiunit signal.…”