Direction-selective single units in the nucleus lentiformis mesencephali of the pigeon (Columba livia)

Winterson, Barbara J.; Brauth, Steven E.

doi:10.1007/bf00235916

Cited by 105 publications

(105 citation statements)

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“…The accessory optic system of birds encodes optic flow produced when an observer moves relative to their environment. Its neurons have wide receptive fields and are directionally biased (14). One of the key accessory optic system nuclei is the lentiformis mesencephali, and it is hypertrophied in all birds capable of hovering, including transient hovering (15).…”

Section: Discussionmentioning

confidence: 99%

“…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.…”

Section: Discussionmentioning

confidence: 99%

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Hummingbirds control hovering flight by stabilizing visual motion

Goller

Altshuler

2014

Proc. Natl. Acad. Sci. U.S.A.

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Relatively little is known about how sensory information is used for controlling flight in birds. A powerful method is to immerse an animal in a dynamic virtual reality environment to examine behavioral responses. Here, we investigated the role of vision during free-flight hovering in hummingbirds to determine how optic flowimage movement across the retina-is used to control body position. We filmed hummingbirds hovering in front of a projection screen with the prediction that projecting moving patterns would disrupt hovering stability but stationary patterns would allow the hummingbird to stabilize position. When hovering in the presence of moving gratings and spirals, hummingbirds lost positional stability and responded to the specific orientation of the moving visual stimulus. There was no loss of stability with stationary versions of the same stimulus patterns. When exposed to a single stimulus many times or to a weakened stimulus that combined a moving spiral with a stationary checkerboard, the response to looming motion declined. However, even minimal visual motion was sufficient to cause a loss of positional stability despite prominent stationary features. Collectively, these experiments demonstrate that hummingbirds control hovering position by stabilizing motions in their visual field. The high sensitivity and persistence of this disruptive response is surprising, given that the hummingbird brain is highly specialized for sensory processing and spatial mapping, providing other potential mechanisms for controlling position. T o precisely control their motion through the air, flying animals have evolved specialized sensory structures and associated neural architecture. Neural specializations provide hypotheses for what senses are most important to a given taxon, and although flight control has been studied extensively in insects (1), birds have until recently received limited attention. Birds have large regions of the brain dedicated to visual processing, suggesting parallels with insects, such as a leading role for optic flow in controlling flight paths (2, 3). It has recently been demonstrated that birds exhibit visually mediated position control much like bees (4, 5), even though they have complex spatial mapping in the hippocampal formation (6), and a much larger brain for interpreting visual input and dynamically integrating vision with proprioceptive and vestibular feedback (7-9).In birds and mammals, the visual information from the eyes is divided into three separate pathways that each process a subset of motions or visual features (10). Two of these pathways, named the accessory optic system and tectofugal pathways in birds, each process a single type of motion: (i) self-or ego-motion, which is the motion produced when an observer moves relative to their environment; and (ii) object motion, when visual features move relative to the observer (2). Using the same retinal information, the visual system of a flying hummingbird must separate motions arising from the bird moving through foliage toward a ...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Hummingbirds control hovering flight by stabilizing visual motion

Goller

Altshuler

2014

Proc. Natl. Acad. Sci. U.S.A.

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“…In pigeons and some other birds, when walking on the ground, a 'headbobbing' reflex also stabilises the head (Dunlap and Mowrer, 1930;Friedman, 1975;Frost, 1978;Davies and Green, 1988;Green et al, 1994;Troje and Frost, 2000;Fujita, 2003). The fundamental role of the nucleus of the optic basal root (nBOR) and the pretectal nucleus lentiformis mesencephali (nLM) in the elaboration of optokinetic responses in birds is well established (Britto et al, 1981;Mc Kenna andWallman, 1981, 1985;Morgan and Frost, 1981;Gioanni et al, 1983aGioanni et al, ,b, 1984Winterson and Brauth, 1985;Telford and Frost, 1989;Frost, 1990a,b, 1999;Wylie et al, 1998a;Frost et al, 1990;Fu et al, 1998a,b;Zhang et al, 1999;Wang et al, 2000a).…”

Section: Introductionmentioning

confidence: 99%

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

Maurice¹,

Gioanni²,

Abourachid³

2006

Journal of Experimental Biology

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'walking', and disappeared in the 'flying' condition. Correlatively, the working range of the OCR (evaluated by its gain at the plateau of SPV) was progressively extended toward higher stimulation velocities.The velocity of the fast phases of the OCR (measured for all the conditions except the 'walking condition') also increased in correlation with the SPV. The walking speed did not influence the OCR in the treadmill velocity range of 0.20-0.40·m·s -1. The presence of a frontal airstream in the 'standing condition' did not change the OCR properties. This fact (and other observations discussed in the paper) suggests that the adaptation of the OCR to the behavioural context is mediated by internal signals generated by each behavioural condition.

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“…Extensive studies on various species have reported that motionsensitive neurons are selective for the direction and speed of visual stimulus motion in the visual cortex (Maunsell and Van Essen, 1983;Petersen et al, 1985;Hammond et al, 1988;Lisberger and Movshon, 1999;Priebe and Lisberger, 2002;Liu and Newsome, 2003) as well as in the pretectum and the accessory optic system (Winterson and Brauth, 1985;Natal and Britto, 1987;Soodak and Simpson, 1988;Hoffmann and Distler, 1989;Mustari and Fuchs, 1989;Frost et al, 1990;Klauer et al, 1990;Wolf-Oberhollenzer and Kirschfeld, 1994;Li et al, 1996;Fu et al, 1998a,b;Zhang et al, 1999;Gu et al, 2001;Ibbotson and Price, 2001;Wang et al, 2001;Clifford and Ibbotson, 2003;Crowder et al, 2003). However, motion is physically described by its acceleration, as well as its direction and speed.…”

Section: Introductionmentioning

confidence: 99%

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

Cao¹,

Gu²,

Wang³

2004

J. Neurosci.

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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 pigeon's 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.

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Direction-selective single units in the nucleus lentiformis mesencephali of the pigeon (Columba livia)

Cited by 105 publications

References 26 publications

Hummingbirds control hovering flight by stabilizing visual motion

Hummingbirds control hovering flight by stabilizing visual motion

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

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

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