Tectal neurons signal impending collision of looming objects in the pigeon

Wu, Le-Qing; Niu, Yu-Qiong; Yang, Jin; Wang, Shurong

doi:10.1111/j.1460-9568.2005.04397.x

Cited by 69 publications

(97 citation statements)

References 35 publications

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“…Previous work on this crab had shown that a robust and reliable escape response could be elicited by computer-generated looming stimuli while two subclasses of previously identified movement-detector neurons from the lobula (third optic neuropil) exhibited robust and consistent responses to the same looming stimuli that trigger the behavioral response (Oliva et al, 2007). These effects were also studied in pigeons, showing a tight correlation between the activity of the rotundal loomingsensitive cells, the muscle activity and the heart rate measurements (Wang and Frost, 1992;Wu et al, 2005). These findings and ours strengthen the idea that in the face of impending danger the crab triggers several integrated defensive reactions.…”

Section: Discussionmentioning

confidence: 94%

The cardiac response of the crabChasmagnathus granulatusas an index of sensory perception

Burnovicz

Oliva

Hermitte

2009

Journal of Experimental Biology

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SUMMARYWhen an animalʼs observable behavior remains unaltered, one can be misled in determining whether it is able to sense an environmental cue. By measuring an index of the internal state, additional information about perception may be obtained. We studied the cardiac response of the crab Chasmagnathus to different stimulus modalities: a light pulse, an air puff, virtual looming stimuli and a real visual danger stimulus. The first two did not trigger observable behavior, but the last two elicited a clear escape response. We examined the changes in heart rate upon sensory stimulation. Cardiac response and escape response latencies were also measured and compared during looming stimuli presentation. The cardiac parameters analyzed revealed significant changes (cardio-inhibitory responses) to all the stimuli investigated. We found a clear correlation between escape and cardiac response latencies to different looming stimuli. This study proved useful to examine the perceptual capacity independently of behavior. In addition, the correlation found between escape and cardiac responses support previous results which showed that in the face of impending danger the crab triggers several coordinated defensive reactions. The ability to escape predation or to be alerted to subtle changes in the environment in relation to autonomic control is associated with the complex ability to integrate sensory information as well as motor output to target tissues. This ʻfear, fight or flightʼ response gives support to the idea of an autonomic-like reflexive control in crustaceans.

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Section: Discussionmentioning

confidence: 94%

The cardiac response of the crabChasmagnathus granulatusas an index of sensory perception

Burnovicz

Oliva

Hermitte

2009

Journal of Experimental Biology

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“…The peak firing rate always occurs a fixed delay after the time at which the looming stimulus reaches an angular threshold on the retina, independent of the stimulus' specific characteristics, such as the simulated object's size, speed, texture, or approach direction (Gabbiani et al, 1999;. Neurons with nearly identical response profiles have been identified in a variety of vertebrate and invertebrate species (Sun and Frost, 1998;Wu et al, 2005;Preuss et al, 2006;Fotowat et al, 2009;Nakagawa and Hongjian, 2010;Liu et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Logarithmic Compression of Sensory Signals within the Dendritic Tree of a Collision-Sensitive Neuron

Jones

Gabbiani²

2012

J. Neurosci.

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Neurons in a variety of species, both vertebrate and invertebrate, encode the kinematics of objects approaching on a collision course through a time-varying firing rate profile that initially increases, then peaks, and eventually decays as collision becomes imminent. In this temporal profile, the peak firing rate signals when the approaching object's subtended size reaches an angular threshold, an event which has been related to the timing of escape behaviors. In a locust neuron called the lobula giant motion detector (LGMD), the biophysical basis of this angular threshold computation relies on a multiplicative combination of the object's angular size and speed, achieved through a logarithmic-exponential transform. To understand how this transform is implemented, we modeled the encoding of angular velocity along the pathway leading to the LGMD based on the experimentally determined activation pattern of its presynaptic neurons. These simulations show that the logarithmic transform of angular speed occurs between the synaptic conductances activated by the approaching object onto the LGMD's dendritic tree and its membrane potential at the spike initiation zone. Thus, we demonstrate an example of how a single neuron's dendritic tree implements a mathematical step in a neural computation important for natural behavior.

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“…Conversely, electrophysiological investigations of neurons underlying looming detection have been performed in relatively few species [e.g. flies (Borst, 1991), hawkmoth (Wicklein and Strausfeld, 2000), goldfish (Gallagher and Northmore, 2006), locust (Gabbiani et al, 2002;Gray, 2005;Rind and Simmons, 1992), pigeon (Wang and Frost, 1992;Wu et al, 2005)], but it is only in locusts where attempts have been made to relate the neuronal activity with an actual behavioral response (e.g. Gray et al, 2001;Santer et al, 2005;Santer et al, 2006).…”

Section: Accepted 4 January 2007mentioning

confidence: 99%

Escape behavior and neuronal responses to looming stimuli in the crabChasmagnathus granulatus(Decapoda: Grapsidae)

Oliva

Medan

Tomsic

2007

Journal of Experimental Biology

123

105

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SUMMARY Behavioral responses to looming stimuli have been studied in many vertebrate and invertebrate species, but neurons sensitive to looming have been investigated in very few animals. In this paper we introduce a new experimental model using the crab Chasmagnathus granulatus, which allows investigation of the processes of looming detection and escape decision at both the behavioral and neuronal levels. By analyzing the escape response of the crab in a walking simulator device we show that: (i) a robust and reliable escape response can be elicited by computer-generated looming stimuli in all tested animals; (ii) parameters such as distance, speed, timing and directionality of the escape run, are easy to record and quantify precisely in the walking device; (iii) although the magnitude of escape varies between animals and stimulus presentations, the timing of the response is remarkably consistent and does not habituate at 3 min stimulus intervals. We then study the response of neurons from the brain of the crab by means of intracellular recordings in the intact animal and show that: (iv) two subclasses of previously identified movement detector neurons from the lobula (third optic neuropil) exhibit robust and reliable responses to the same looming stimuli that trigger the behavioral response; (v) the neurons respond to the object approach by increasing their rate of firing in a way that closely matches the dynamics of the image expansion. Finally, we compare the neuronal with the behavioral response showing that: (vi) differences in the neuronal responses to looming, receding or laterally moving stimuli closely reflect the behavioral differences to such stimuli; (vii) during looming, the crab starts to run soon after the looming-sensitive neurons begin to increase their firing rate. The increase in the running speed during stimulus approach faithfully follows the increment in the firing rate, until the moment of maximum stimulus expansion. Thereafter, the neurons abruptly stop firing and the animal immediately decelerates its run. The results are discussed in connection with studies of responses to looming stimuli in the locust.

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Tectal neurons signal impending collision of looming objects in the pigeon

Cited by 69 publications

References 35 publications

The cardiac response of the crabChasmagnathus granulatusas an index of sensory perception

The cardiac response of the crabChasmagnathus granulatusas an index of sensory perception

Logarithmic Compression of Sensory Signals within the Dendritic Tree of a Collision-Sensitive Neuron

Escape behavior and neuronal responses to looming stimuli in the crabChasmagnathus granulatus(Decapoda: Grapsidae)

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