Spatiotemporal Frequency Tuning Dynamics of Neurons in the Owl Visual Wulst

Abstract

The transformation of spatial (SF) and temporal frequency (TF) tuning functions from broad-band/low-pass to narrow band-pass profiles is one of the key emergent properties of neurons in the mammalian primary visual cortex (V1). The mechanisms underlying such transformation are still a matter of ongoing debate. With the aim of providing comparative insights into the issue, we analyzed various aspects of the spatiotemporal tuning dynamics of neurons in the visual wulst of four awake owls. The wulst is the avian telencephalic target of the retinothalamofugal pathway and, in owls, bears striking functional analogy with V1. Most neurons in our sample exhibited fast and large-magnitude adaptation to the visual stimuli with response latencies very similar to those reported for V1. Moreover, latency increased as a function of stimulus SF but not TF, which suggests that parvo- and magno-like geniculate inputs could be converging onto single wulst neurons. No net shifts in preferred SF or TF were observed along the initial second of stimulation, but bandwidth decreased roughly during the first 200 ms after response latency for both stimulus dimensions. For SF, this occurred exclusively as a consequence of low-frequency suppression, whereas suppression was observed both at the low- and high-frequency limbs of TF tuning curves. Overall these results indicate that SF and TF tuning curves in the wulst are shaped by both feedforward and intratelencephalic suppressive mechanisms, similarly to what seems to be the case in the mammalian striate cortex.

Speed-Selectivity in Retinal Ganglion Cells is Sharpened by Broad Spatial Frequency, Naturalistic Stimuli

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Dynamics of spatial frequency tuning in mouse visual cortex

“…9). In the burrowing owl wulst, this shift in LSFS was also observed although it was accompanied by a decrease in tuning bandwidth but not by a change in the preferred spatial frequency (Pinto and Baron 2010). We did not analyze tuning bandwidth, since we knew from earlier studies that up to 30% of mouse units showed low pass tuning for spatial frequency (Van den Bergh et al 2010) and would thus provide no useful metric for this property.…”

“…While these spatial frequency tuning dynamics are clearly observable in the primary visual cortex, they might partly originate in the lateral geniculate nucleus (LGN) (Allen and Freeman 2006). In the wulst of the burrowing owl, a V1 analog in birds, similar temporal changes in spatial frequency tuning were observed without a parallel shift in preferred spatial frequency (Pinto and Baron 2010).…”

Pigeons use low rather than high spatial frequency information to make visual category discriminations.

“…The idea of separate channels for different spatial frequencies within the vertebrate visual system has been a powerful one, and it continues to be deployed, not least in relation to the visual systems of birds (e.g.. Pinto & Baron, 2010). It seems, however, that further investigation of the psychophysical and cognitive roles of such channels is required.…”