Shu-Rong Wang

Visual Responses of Neurons in the Pretectal Nucleus lentiformis mesencephali to Moving Patterns Within and Beyond Receptive Fields in Pigeons

Large-field patterns are effective stimuli for eliciting visual responses from neurons in the pretectal nucleus lentiformis mesencephali of nonmammals. The present study shows that stimulation beyond the receptive field does not contribute to the visual responses of neurons in the nucleus lentiformis mesencephali in two respects. First, changes in the direction and velocity of motion beyond the receptive field did not affect the visual responses of the pretectal cells to motion within the receptive field. Second, time differences in the onset of stimulation within and outside the receptive field did not influence the visual responses of the pretectal cells to motion in the receptive field, implying that there may be no long-range interaction between the receptive field and its surrounding field. The present study also indicates that the pretectal cells are not only sensitive to the direction and velocity of motion, but also to the size and density of dots in a random-dot pattern moving through the receptive field. Taken together with previous studies, these results suggest that the receptive field of the pretectal cells within the nucleus lentiformis mesencephali is large in size but well defined in boundaries, and that the pretectal cells respond to motion of visual stimuli within but not beyond their receptive fields.

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

Seeing target motion is a vital capability of the visual system in humans and animals. Physically, motion is described by its acceleration, speed, and direction. Motion-sensitive neurons in all the visual areas examined to date are selective for the direction and speed of motion. Here, we show by single-unit recording that one-third of motion-sensitive neurons in the pigeons pretectal nucleus also encode the acceleration of stimulus motion. These neurons are characterized by plateau-shaped speed-tuning curves in which the firing rate is the same over a wide range of speeds, a feature that allows these neurons to encode unambiguously the rate of change of speed over time. Acceleration-sensitive neurons also show transient responses to the offset of motion in the preferred and/or nonpreferred directions; acceleration-insensitive neurons do not. We observed the same sensitivity to target acceleration for brief ramps of stimulus speed and for sinusoidal modulation of speed. The locations of acceleration-sensitive and -insensitive neurons are segregated in the pretectal nucleus. The visual responses of pretectal neurons indicate that the visual and vestibular systems share not only a spatial but also a temporal reference frame that can detect the acceleration produced by self-motion of an organism.

Looming-sensitive responses and receptive field organization of telencephalic neurons in the pigeon

The tectofugal pathway in birds goes from the optic tectum to the telencephalic entopallium via the thalamic nucleus rotundus (nRt). This pathway may be homologous to the colliculo-pulvinar-cortical pathway in mammals. It is known that a population of rotundal neurons in the pigeon can signal impending collision of looming objects with the animal. Here we show by single-unit recording that there exist two groups of looming-sensitive neurons in the entopallium. A tau cell starts firing at a nearly constant time before collision whereas the response onset time of an eta cell is linearly related to the square root of the diameter/velocity ratio of looming objects. These cells are localized in the caudal entopallium. The receptive field (RF) of looming-sensitive cells was mapped on the screen plane but its inhibitory region could not suppress responses to looming objects. It appears that a population of telencephalic cells in pigeons responds to looming objects and their looming responses are not determined by the receptive field organization mapped on the screen plane.

Stimulus features eliciting visual responses from neurons in the nucleus lentiformis mesencephali in pigeons.

The purpose of the present study was to find out what particular stimulus features, in addition to the direction and velocity of motion, specifically activate neurons in the nucleus lentiformis mesencephali (nLM) in pigeons. Visual responses of 60 nLM cells to a variety of computer-generated stimuli were extracellularly recorded and quantitatively analyzed. Ten recording sites were histologically verified to be localized within nLM with cobalt sulfide markings. It was shown that the pigeon nLM cells were specifically sensitive to the leading edge moving at the optimal velocity in the preferred direction through their excitatory receptive fields (ERFs). Generally speaking, nLM cells preferred black edges to white ones. However, this preference cannot be explained by OFF-responses to a light spot. The edge sharpness was also an essential factor influencing the responsive strength, with blurred edges producing little or no visual responses at all. These neurons vigorously responded to black edge orientated perpendicular to, and moved in, the preferred direction; the magnitude of visual responses was reduced with changing orientation. The spatial summation occurred in all neurons tested, characterized by the finding that neuronal firings increased as the leading edge was lengthened until saturation was reached. On the other hand, it appeared that nLM neurons could not detect any differences in the shape and area of stimuli with an identical edge. These data suggested that feature extraction characteristics of nLM neurons may be specialized for detecting optokinetic stimuli, but not for realizing pattern recognition. This seems to be at least one of the reasons why large-field gratings or random-dot patterns have been used to study visual responses of accessory optic neurons and optokinetic nystagmus, because many high-contrast edges in these stimuli can activate a neuron to periodically discharge, or groups of neurons to simultaneously fire to elicit optokinetic reflex.

Avian Imc-tectal projection is mediated by acetylcholine and glutamate

In the bird, biochemical and histochemical data suggest that the neurotransmitter between nucleus isthmi pars magnocellularis (Imc) and tectum is either acetylcholine or glutamate. There are, however, discrepancies regarding the functional role of acetylcholine. In the present study we investigated the action of acetylcholine and glutamate and their specific antagonists on excitatory isthmo-tectal synaptic transmission using electrophysiological and microiontophoretic techniques. The results show two different population of cells: (1) excitatory cholinergic input, blocked by atropine sulphate but not by glutamate antagonist; (2) excitatory glutamatergic input of NMDA or non-NMDA receptor type, which is blocked or reduced by CPP or CNQX but not by atropine sulphate.

Corollary discharge circuits for saccadic modulation of the pigeon visual system.

A saccadic eye movement causes a variety of transient perceptual sequelae that might be the results of corollary discharge. Here we describe the neural circuits for saccadic corollary discharge that modulates activity throughout the pigeon visual system. Saccades in pigeons caused inhibition that was mediated by corollary discharge followed by enhancement of firing activity in the telencephalic hyperpallium, visual thalamus and pretectal nucleus lentiformis mesencephali (nLM) with opposite responses in the accessory optic nucleus (nBOR). Inactivation of thalamic neurons eliminated saccadic responses in telencephalic neurons, and inactivation of both the nLM and the nBOR abolished saccadic responses in thalamic neurons. Saccade-related omnipause neurons in the brainstem raphe complex inhibited the nBOR and excited the nLM, whereas inactivation of raphe neurons eliminated saccadic responses in both optokinetic and thalamic neurons. It seems that saccadic responses in telencephalic neurons are generated by corollary discharge signals from brainstem neurons that are transmitted through optokinetic and thalamic neurons. These signals might have important roles in visual perception.

RECEPTIVE FIELD CHARACTERISTICS OF NEURONS IN THE NUCLEUS OF THE BASAL OPTIC ROOT IN PIGEONS

Optokinetic nystagmus is a reflex to stabilize an object image on the retina by compensatory eye movements. In lower vertebrates, the nucleus of the basal optic root participates in generating this reflex. Visual responses of 135 neurons were extracellularly recorded from the nucleus in pigeons and their receptive field properties were analysed on-line with a workstation. These cells could be categorized into slow (84%), intermediate (3%) and fast (13%) cells, preferring motion velocities of 0.25-8, 16 and 32-64 deg./s, respectively. Using whole-field gratings as stimuli revealed that 97% of the cells were selective for direction of motion and 3% were not. The directional cells preferred motion in the dorsoventral (35%), nasotemporal (34%), ventrodorsal (23%), or temporonasal (8%) directions. The omni-directional neurons were equally excited or inhibited by motion in all directions. The receptive field of basal optic neurons usually consisted of an excitatory receptive field and an inhibitory receptive field, both of which possessed opposite (heterodirectional) or identical (homodirectional) directionalities. In the case of homodirectional co-existence of both fields, whether whole-field gratings could produce visual responses from the cells would depend on the interaction between excitation and inhibition evoked in their excitatory and inhibitory receptive fields, respectively. Therefore, in some cases a single object was more effective than whole-field gratings in eliciting visual responses from basal optic neurons in pigeons. All of these receptive field properties revealed by on-line computer analysis may underlie the detection of optic flow and the induction of optokinetic responses.

Visual responses of neurons in the avian nucleus isthmi.

Electrophysiological responses of neurons to visual and auditory stimulation are extracellularly recorded from the pigeon isthmic area. Cobalt sulfide markings show that only visual units are localized within the nucleus isthmi pars parvocellularis (Ipc) and pars magnocellularis (Imc), while visual-auditory bimodal units are localized outside. Visual units respond to black or white targets moving through their receptive fields (RFs). The RF centers are mainly distributed in the contralaterally lower visual field. The rostral Ipc and Imc receive information from the nasal visual field, and the caudal part of the Ipc and Imc corresponds to the temporal field. Therefore, both Ipc and Imc are visual centers instead of auditory centers as described before.

Centrifugal innervation modulates visual activity of tectal cells in pigeons

Centrifugal modulation of visual responsiveness of tectal cells by the isthmo-optic nucleus (ION) through the retina was studied in homing pigeons. Visual activity evoked by computer-generated stimuli was reduced by an average of 59% in tectal cells whose receptive fields (RFs) either overlapped with, or were close to, those of isthmo-optic cells whose activity was blocked by the injection of lidocaine through micropipettes. Activity usually recovered to 87% of pre-drug controls in 8-17 min (average 12.3 min) after stopping lidocaine injections. Those tectal cells whose RFs were far from those of ION cells did not show clear-cut changes in their visual responsiveness to isthmo-optic lidocaine application. The spatial relationship between receptive fields of tectal and isthmo-optic cells, saline controls, as well as the specificity, reproducibility and reversibility of effects of ION-injected lidocaine on tectal activity, show that this chemical action is pharmacological, not toxicological. Neuronal circuitry underlying centrifugal modulation of tectal activity by isthmo-optic cells is discussed.

Excitatory and inhibitory neurotransmitters in the nucleus rotundus of pigeons

Rotundal neurons in pigeons (Columba livia) were examined for the effects of glutamate and its agonists NMDA and AMPA, antagonists CPP and CNQX, as well as of GABA and its antagonist bicuculline, on visual and tectal stimulation-evoked responses. Glutamate applied by iontophoresis excited all 48 rotundal cells tested, and this excitation was blocked by CNQX but not by CPP in 98% of cases, with 2% of cells being blocked by either CNQX or CPP. Out of 21 cells excited by AMPA, 20 were also excited by NMDA, indicating that AMPA and NMDA receptors may coexist in most rotundal cells. Action potentials were evoked in 36 additional cells by electrical stimulation applied to the tectum and they were also blocked by CNQX but not CPP. Visual responses recorded from a further eight luminance units and 21 motion-sensitive units were also blocked by CNQX and not CPP. On the other hand, GABA inhibited visual responses as well as responses evoked by tectal stimulation. An inhibitory period following tectal stimulation was eliminated by bicuculline. Taken together, these results indicate that glutamate may be an excitatory transmitter acting predominantly through non-NMDA receptors (AMPA receptors) in tectorotundal transmission. Meanwhile, GABA may be an inhibitory transmitter in the pigeon nucleus rotundus.