Neuroethology of a releasing mechanism

As with other vertebrates, early visual processing in amphibians takes place in the neuronal circuits of the retina. The neurons of the vertebrate retina (see Fig. 2.4, p. 25, and Box 5.1, p. 107) are arranged in a way that provides for both lateral interaction and through transmission. The through route of the visual pathway is made up of receptors, bipolar cells and ganglion cells.

Recording with microelectrodes shows that the receptors respond in a simple way to changes in the intensity of light that falls on them as part of the image formed by the eye. These responses are mirrored by the bipolar cells, each of which receives input from several receptors. In turn, the ganglion cells each pool input received from a large number of bipolar cells. The ganglion cells are able to respond to more complex features of the image because of the way information from the receptors is processed and combined on its way to the ganglion cells. Ganglion cells can be divided into several different classes on the basis of the type of feature to which each is most sensitive. Some are most sensitive to objects of a given angular size, others to objects moving in a particular direction or to the difference in brightness between adjacent areas of the image. This information is passed along the optic nerve to the brain (Fig. 1.5), where these basic parameters are used to distinguish between mate, prey and predator.

The majority of retinal ganglion cells are connected to the optic tectum, a specialised region of the midbrain visible as a large bulge on either side (Fig. 1.5). A smaller number of ganglion cells are connected to the thalamus, which is the most prominent part of the posterior forebrain, and to the pretectal areas of the midbrain. These connections are spread out in an

Tectum

Tectum

Toad Tectum

Figure 1.5 The layout of the main visual pathways concerned in prey detection in the brain of an anuran amphibian. The axons of most ganglion cells travel from the eye to the optic tectum on the opposite (contralateral) side of the brain, via the optic nerve (other cranial nerves are not shown). Feature-detecting neurons of the optic tectum send their axons to the motor regions of the contralateral hindbrain.

Hindbrain p — Optic Forebrain nerve

Figure 1.5 The layout of the main visual pathways concerned in prey detection in the brain of an anuran amphibian. The axons of most ganglion cells travel from the eye to the optic tectum on the opposite (contralateral) side of the brain, via the optic nerve (other cranial nerves are not shown). Feature-detecting neurons of the optic tectum send their axons to the motor regions of the contralateral hindbrain.

orderly manner in the superficial layer of the optic tectum, with each ganglion cell keeping the same relative position with respect to its neighbours that it has in the retina.

The responses of the tectal neurons can be recorded by probing the deeper layers of the optic tectum with a microelectrode (Fig. 1.6). Like the ganglion cells, the neurons of the thalamus and tectum can be divided into different classes according to their patterns of response. Of the thalamic and tectal neurons that have been investigated, at least three classes show differing responses to moving stimuli of worm and antiworm configurations. The thalamic Class TH3 neurons respond best to squares; stripes with the antiworm configuration elicit a lesser response, and the worm configuration elicits the least response of all (Fig. 1.6fc). In the optic tectum, the Class T5(1) neurons also respond best to squares, but when tested with stripes, they prefer the worm to the antiworm configuration (Fig. 1.6c). Another class of tested cells, the Class T5(2) neurons, distinguish much more clearly between the worm and antiworm configurations, with the worm configuration eliciting the greatest response, the squares a lesser response, and the antiworm by far the least response (Fig. 1.6d). Among all the neurons tested so far, the response pattern of the T5(2) neurons shows

Figure 1.6 (a) Set-up for recording the responses of neurons in the brain to moving visual stimuli. The toad is held in a fixed position and its brain is probed with a microelectrode for recording the spikes in single neurons. Each stimulus is moved in front of the toad by means of the perimeter device. (b) The response of thalamic Class TH3 neurons to increasing angular size of the same three shapes (x, y, z) used in the behavioural tests (Fig. 1.4). (c) The response of tectal Class T5(1) neurons to the same three shapes. (d) The response of tectal Class T5(2) neurons to the same shapes. (a redrawn after Ewert, 1985; b-d redrawn after Ewert, 1980.)

Figure 1.6 (a) Set-up for recording the responses of neurons in the brain to moving visual stimuli. The toad is held in a fixed position and its brain is probed with a microelectrode for recording the spikes in single neurons. Each stimulus is moved in front of the toad by means of the perimeter device. (b) The response of thalamic Class TH3 neurons to increasing angular size of the same three shapes (x, y, z) used in the behavioural tests (Fig. 1.4). (c) The response of tectal Class T5(1) neurons to the same three shapes. (d) The response of tectal Class T5(2) neurons to the same shapes. (a redrawn after Ewert, 1985; b-d redrawn after Ewert, 1980.)

the best correlation with the sign stimuli for prey-catching behaviour (cf. Fig 1.6d and Fig. 1.4b).

It is evident from Fig. 1.6 that the responses of the Class T5(2) neurons could be accounted for if they receive excitatory input from Class T5(1) neurons and inhibitory input from Class TH3 neurons. The fairly strong response to the worm configuration in Class T5(1) neurons would be minimally inhibited by the poor response to it in the Class TH3 neurons, resulting in a strong response in the Class T5(2) neurons. Similarly, the poor response to the antiworm configuration in Class T5(1) would interact with the moderate response in Class TH3 to give a very poor response in Class T5(2).

This possibility has been tested by removing the input from the Class TH3 neurons, which can be accomplished by severing the pathway that is known to run from the thalamus to the optic tectum. Whether this lesion is done permanently by microsurgery or temporarily by local application of a neurotoxin, the effect on Class T5(2) neurons is dramatic. The responsiveness of these neurons to all visual stimuli is increased and selectivity is lost, with the neurons responding best to squares and failing to distinguish clearly between stripes in worm and antiworm configurations. This shows that the normal selective response of the Class T5(2) neurons is dependent on inhibition from thalamic neurons, including the Class TH3 neurons.

When a toad with a pretectal lesion is allowed to recover from surgery and is tested behaviourally, its responses closely parallel those of the T5(2) neurons: the operated animal responds vigorously to all shapes, preferring squares and failing to distinguish clearly between worm and antiworm configurations of stripes. Such a close correspondence between the responses of the Class T5(2) neurons and of the whole animal suggests that these neurons are directly involved in prey detection and hence in releasing prey-catching activity. This is confirmed by means of a small telemetry system that enables the experimenter to record from and stimulate single neurons in the optic tectum of a freely moving toad. Recordings made with this system show that activity of Class T5(2) neurons precedes and continues during the orientation of the toad towards the prey. Having recorded in detail from a particular T5(2) neuron, it can then be stimulated by passing a tiny current through the microelectrode, and this consistently elicits orientating movements that are directed to the appropriate part of the visual field.

If they are involved in prey detection in this way, one would expect the Class T5(2) neurons to be connected, directly or indirectly, with the motor circuits in the hindbrain of the toad. Various histological methods demonstrate that a number of the connections arriving in the motor regions on one side of the hindbrain do come from the contralateral optic tectum (see

Fig. 1.5). That these include the Class T5(2) neurons is confirmed by physiological methods. Localised stimulation of the appropriate neural tract in the hindbrain sends signals travelling back up to the optic tectum, where they can be recorded in individual T5(2) neurons with a microelectrode.

Thus, the Class T5(2) neurons provide an excellent example of specific brain cells that are involved in releasing a simple, important behaviour pattern. On the basis of the stimulus parameters selected by the retinal ganglion cells, the neurons of the optic tectum are able to respond to specific parameter combinations that carry information relevant to the toad's way of life. The specific combination of visual parameters to which the T5(2) neurons respond carries information enabling the toad to distinguish between its natural prey and inedible objects. These response properties of the T5(2) neurons do not identify worms or beetles, but rather they underlie the sign stimuli that elicit prey-catching behaviour in a hungry toad.

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