Auditory and Multisensory Responses in the Tectofugal Pathway of the Barn Owl

Abstract

A common visual pathway in all amniotes is the tectofugal pathway connecting the optic tectum with the forebrain. The tectofugal pathway has been suggested to be involved in tasks such as orienting and attention, tasks that may benefit from integrating information across senses. Nevertheless, previous research has characterized the tectofugal pathway as strictly visual. Here we recorded from two stations along the tectofugal pathway of the barn owl: the thalamic nucleus rotundus (nRt) and the forebrain entopallium (E). We report that neurons in E and nRt respond to auditory stimuli as well as to visual stimuli. Visual tuning to the horizontal position of the stimulus and auditory tuning to the corresponding spatial cue (interaural time difference) were generally broad, covering a large portion of the contralateral space. Responses to spatiotemporally coinciding multisensory stimuli were mostly enhanced above the responses to the single modality stimuli, whereas spatially misaligned stimuli were not. Results from inactivation experiments suggest that the auditory responses in E are of tectal origin. These findings support the notion that the tectofugal pathway is involved in multisensory processing. In addition, the findings suggest that the ascending auditory information to the forebrain is not as bottlenecked through the auditory thalamus as previously thought.

Stimulus-Specific Adaptation: Can It Be a Neural Correlate of Behavioral Habituation?

“…We report a new form of neural adaptation that has a relatively long memory trace (up to a minute and possibly more) and is stimulus specific. We further show that this form of adaptation is absent in the ascending auditory pathway to the OT and in the primary auditory thalamus, but is apparent, in addition to the OT, in the entopallium (E), a forebrain area connected to the gaze control system (Benowitz and Karten, 1976;Reches and Gutfreund, 2009). We therefore propose that gaze control circuitry, which is involved in the selection of salient stimuli in space (Boehnke and Munoz, 2008;Mysore et al, 2010), is also involved in the selection of salient stimuli in time.…”

“…This area was characterized by a high level of spontaneous bursty activity and strong responses to visual stimuli. The correspondence of the stereotaxic coordinates and the characteristic physiological responses with the desired brain locations were previously confirmed with anatomical reconstructions of the recording sites (Knudsen, 1982;Wagner et al, 1987;Brainard and Knudsen, 1993;Gutfreund et al, 2002;Miller and Knudsen, 2003;Pérez and Peña, 2006;Reches and Gutfreund, 2009;Netser et al, 2010). In all nuclei, the electrode was advanced within the nucleus in 300 m steps; at each step, basic auditory responses (frequency, ITD, ILD) and visual responsiveness were first measured to make sure that the recording site is within the desired nucleus.…”

“…The E was targeted 2 mm rostral, 0.4 mm lateral, and 6.5-7 mm dorsal from the same tectal reference point. In the E, we recorded in the area in which we have previously identified auditory responses (Reches and Gutfreund, 2009). This area was characterized by a high level of spontaneous bursty activity and strong responses to visual stimuli.…”

Stimulus-specific adaptation, habituation and change detection in the gaze control system

“…Mounting evidence shows that the OT/SC contains more than a simple motor system. Information from the OT/SC is also sent to a wide range of cortical and basal ganglia regions via thalamic nuclei (Robinson and Petersen 1992;Takada et al 1985;Bischof and Watanabe 1997;Reches and Gutfreund 2009). An emerging hypothesis is that the evolutionary role of the OT/SC is to sort stimuli based on saliency, select the most salient stimulus, and send this information to the appropriate brain regions to direct orienting movements, attention, and autonomic responses (Review in Boehnke and Munoz 2008;Knudsen 2011).…”

“…In barn owls, this region receives visual and auditory inputs originating in the OT ( Fig. 2; Reches and Gutfreund 2009). Nevertheless, its neurons are far more sensitive to visual stimuli compared to auditory stimuli.…”