Spatiotemporal Properties of Fast and Slow Neurons in the Pretectal Nucleus Lentiformis Mesencephali in Pigeons

Abstract

Neurons in the pretectal nucleus lentiformis mesencephali (LM) are involved in the analysis of optic flow that results from self-motion. Previous studies have shown that LM neurons have large receptive fields in the contralateral eye, are excited in response to largefield stimuli moving in a particular (preferred) direction, and are inhibited in response to motion in the opposite (anti-preferred) direction. We investigated the responses of LM neurons to sine wave gratings of varying spatial and temporal frequency drifting in the preferred and anti-preferred directions. The LM neurons fell into two categories. "Fast" neurons were maximally excited by gratings of low spatial [0.03-0.25 cycles/ degrees (cpd)] and mid-high temporal frequencies (0.5-16 Hz). "Slow" neurons were maximally excited by gratings of high spatial (0.35-2 cpd) and low-mid temporal frequencies (0.125-2 Hz). Of the slow neurons, all but one preferred forward (temporal to nasal) motion. The fast group included neurons that preferred forward, backward, upward, and downward motion. For most cells (81%), the spatial and temporal frequency that elicited maximal excitation to motion in the preferred direction did not coincide with the spatial and temporal frequency that elicited maximal inhibition to gratings moving in the anti-preferred direction. With respect to motion in the anti-preferred direction, a substantial proportion of the LM neurons (32%) showed bi-directional responses. That is, the spatiotemporal plots contained domains of excitation in addition to the region of inhibition. Neurons tuned to stimulus velocity across different spatial frequency were rare (5%), but some neurons (39%) were tuned to temporal frequency. These results are discussed in relation to previous studies of the responses of neurons in the accessory optic system and pretectum to drifting gratings and other largefield stimuli.

Influence of the behavioural context on the optocollic reflex (OCR) in pigeons (Columba livia)

“…In pigeons, nBOR cells are tuned by the spatio-temporal frequency (TF/SF) rather than by their angular velocity of stimuli (WolfOberhollenzer andKirschfeld, 1990, 1994). Similar experiments using a broader range of spatial frequencies have been carried out in the nBOR, the nLM (nucleus lentiformis mesencephali) and the vestibulo-cerebellum of pigeons (Wylie and Crowder, 2000;Crowder et al, 2003a;Winship et al, 2005). These experiments led to the definition of two types of cells found in the three structures: the 'slow neurones', which are most activated by gratings of high SFs (0.35-2.0·cycles·deg. )…”

Hummingbirds control hovering flight by stabilizing visual motion

“…An example of variable sensory integration comes from restrained pigeons that exhibit different head stabilization reflexes and tail responses to visual and vestibular perturbations during simulated flight than during resting conditions (16,17). At the level of sensory neurons, cells of the avian accessory optic system are divided into populations that differ in maximum sensitivity to either fast or slow motion (14,18,19). The functional roles and the relative abundance and distribution of fast and slow cells have not been described in any bird.…”

Visual Neurons in the Pigeon Brain Encode the Acceleration of Stimulus Motion

“…However, the transient/sustained ratios at the onset of motion in the preferred direction were larger in the accelerationsensitive neurons, and the value of the transient/sustained ratio was related to the amount of acceleration responsiveness, indicating that part of the transient is related to the presence of response to stimulus acceleration. Previous studies have shown that many directional cells produce transient responses to the onset of motion (Ibbotson et al, 1998;Lisberger and Movshon, 1999;Wylie and Crowder, 2000;Priebe and Lisberger, 2002) and to the appearance of a stationary pattern (Müller et al, 2001;Gu et al, 2002). The onset transients in these cases could convey information about stimulus motion or edge detection (Awatramani and Slaughter, 2000) and may originate from the retinal bipolar cells and/or some synaptic mechanisms (Awatramani and Slaughter, 2000;Müller et al, 2001).…”

“…We have added an additional parallel between the vestibular and visual neurons in the optokinetic system. They are both sensitive to acceleration, although their physiological modalities (mechanical vs. visual) are quite different (Klinke, 1978;Fu et al, 1998a,b;Wylie and Crowder, 2000;Ibbotson and Price, 2001). …”

“…Self-motion of an organism is also monitored by the vestibular system, and there are a number of spatial and temporal similarities between the responses of vestibular afferent neurons to self-motion and the responses of neurons in the optokinetic system to image motion. Both have high levels of spontaneous activity, and both are characterized by excitatory responses to motion in one direction and inhibitory responses to motion in the opposite direction of adequate stimuli (Klinke, 1978;Fu et al, 1998a,b;Wylie and Crowder, 2000;Ibbotson and Price, 2001). Furthermore, the visual responses of optokinetic neurons seem to be organized in the same spatial coordinate frame as the semicircular canals of the vestibular apparatus (Miles, 1984;Wylie et al, 1998).…”