Review
Neural modulation of visuomotor functions underlying prey-catching behaviour in anurans: perception, attention, motor performance, learning

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Abstract

The present review points out that visuomotor functions in anurans are modifiable and provides neurophysiological data which suggest modulatory forebrain functions. The retino-tecto/tegmento-bulbar/spinal serial processing streams are sufficient for stimulus–response mediation in prey-catching behaviour. Without its modulatory connections to forebrain structures, however, these processing streams cannot manage perceptual tasks, directed attention, learning performances, and motor skills. (1) Visual prey/non-prey discrimination is based on the interaction of this processing stream with the pretectal thalamus involving the neurotransmitter neuropeptide-Y. (2) Experiments applying the dopamine agonist apomorphine in combination with 2DG mapping and single neurone recording suggest that prey-catching strategies in terms of hunting prey and waiting for prey depend on dose dependent dopaminergic adjustments in the neural macronetwork in which retinal, pretecto-tectal, basal ganglionic, limbic, and mesolimbic structures participate. (3) Visual response properties of striatal efferent neurones support the concept that ventral striatum is involved in directed attention. (4) Various modulatory loops involving the ventral medial pallium modify prey-recognition in the course of visual or visual-olfactory learning (associative learning) or are responsible for stimulus-specific habituation (non-associative learning). (5) The circuits suggested to underlie modulatory forebrain functions are accentuated in standard schemes of the neural macronetwork. These provide concepts suitable for future decisive experiments.

Introduction

In the animal kingdom, the modes of acquiring food and consuming it show a great variety and various degrees of complexity. Comparing the procedures of food-intake in a greedy toad and a dining gourmet, we can confidently argue that the differences have something to do with the phylogenetic level of the species and the complexity of the brain. However, principles of variability and complexity of behaviour are not necessarily based on levels of brain organisation. Even a small neuronal network consisting of a countable number of neurons — such as the crustacean stomatogastric ganglion, whose pyloric and gastric subunits control the chewing movements of the stomach — may display a relatively high degree of variability depending on modulatory influences (e.g. see Marder and Hooper, 1985, Marder, 1986, Marder, 1998, Blitz et al., 1999, Fenelon et al., 1999). What can we expect from the brain of a common toad (Fig. 1) — a basal tetrapod vertebrate — regarding the mediation and modulation of feeding?

Anuran amphibians respond to certain visual moving stimuli with prey-catching behaviour, but also other senses can be involved, such as olfactory, gustatory, and somatosensory. Fig. 2C shows how the toad's prey-catching activity changes if significant configurational parameters (edge length parallel to, ep, and/or edge length across, ea, the direction of movement) are varied. Although there are certainly other features describing different types of prey, this simple dummy-test has the advantage of a quantifiable paradigm that allows one to check, e.g. correlations with neuronal responses, influences by learning or effects of brain lesions.

The toad's prey-catching shows various sequential responses: orientational turning towards prey, approaching prey, fixating and snapping it. The stimulus–response chain is variable and depends on the behaviour of the prey, e.g. its location in space. Frogs often orient and snap in one smooth event. Toads Bufo bufo and frogs Rana esculenta apply different prey capture strategies (Eibl-Eibesfeldt, 1951). Common toads are active foragers, hunting prey by orienting, pursuing, fixating, and snapping. The preying success takes advantage of the hunter's locomotory mobility but at the risk of being itself attacked by predators. In the hunting strategy, the discrimination between prey and non-prey is relatively selective. Rana esculenta, a sit-and-wait predator, waits for prey safely at a hiding place where prey density is relatively high. In the waiting strategy, the preying success depends on a relatively low snapping threshold at the disadvantage of catching non-prey items occasionally also. Both in toads and frogs, modulatory adjustments in the brain may also allow transitions from waiting to hunting and vice versa.

Although orienting and snapping movements are primarily ballistic, internal modulatory feedback loops enrich their variability in adaptation to sensory and motor tasks (Gans, 1961, Nishikawa and Gans, 1992). Nishikawa and co-workers suggest that afferent information from the tongue interacts with visual input in controlling prey-catching movements; the prey-catching mode also depends on the kind of prey (Anderson, 1993, Anderson and Nishikawa, 1993, Anderson and Nishikawa, 1996, Anderson and Nishikawa, 1997a, Anderson and Nishikawa, 1997b, Weerasuriya et al., 1994, Valdez and Nishikawa, 1997).

As regards non-visual cues, orienting and snapping can be elicited by tactile stimuli to the snout, the forelimbs or the hindlimbs (Grobstein et al., 1983). Olfactory and gustatory cues in combination with visual prey features play a role in the course of learning by which the innate prey-recognition system can be modified, i.e. either generalised or specified (Ewert, 1968; Ewert, 1991, Shinn and Dole, 1978, Shinn and Dole, 1979, Dole et al., 1981, Merkel-Harff, 1991). The red earthworm Eisenia foetida is distasteful to toads, so that toads store this negative information and retrieve it when faced with this kind of worm (Heusser, 1958). Comparable observations have been reported for toads following prey experience with bombardier beetles (Dean, 1980a, Dean, 1980b). Toads may also associate the visual appearance of a hive bee with the painful sting they received after the bee had been snapped (Cott, 1936; see also Brower et al., 1960, and Brower and Brower, 1962). Hive bees are very distasteful to frogs and toads, so that gustatory stimuli may also set cues of negative experience.

Fig. 1 depicts some neural structures and their verified anatomic connections in the anuran brain. The neural network mediates between visual and olfactory input, on the one hand, and motor output related to prey-orienting and snapping on the other hand. All structures are indirectly, and in part directly, connected with each other. Stimulus response mediation and its modulation take advantage of different computational principles, involving parallel distributed processing of information, converging and diverging processing streams, and feedforward and feedback loops. The task of the present review is to gain an insight into the physiological processes of this macronetwork that are responsible for stimulus–response mediation and their modulation involving the forebrain. We select the following themes:

  • 1.

    The neural circuit that mediates between prey stimulus and prey-catching behaviour consists of retina-fed tectal/tegmental pathways and corresponding rhombencephalic/spinal nuclei.

  • 2.

    The distinction between prey and non-prey is based on interactions of these pathways with diencephalic pretectal structures.

  • 3.

    Directed attention, i.e. the translation of perception into action, are based on modulating forebrain loops which involve the telencephalic striatum.

  • 4.

    Dopaminergic modulations in the macronetwork are suitable to alter prey-catching strategies in terms of hunting prey and waiting for prey.

  • 5.

    Modifications of prey recognition in the course of visual and olfactory learning take advantage of various modulating forebrain loops that involve the telencephalic ventromedial (hippocampal) pallium.

Section snippets

Brain regions ‘dispensible’ for stimulus–response mediation

Is the forebrain dispensible for the mediation between prey stimulus and prey-catching? Data from brain-lesioned toads suggest that the fundamental stimulus–responses are mediated by the retino-tecto/tegmento-bulbar/spinal pathways, in connection with the hypothalamus/pituitary system which maintains the vegetative functions (Fig. 3). After ablation of both telencephalic hemispheres and bilateral removal of the dorsal diencephalon — by sparing the eyes, optic nerves, and optic chiasm, preoptic

Pretecto-tectal projection neurones

Diencephalic lesion studies in toads showed (Ewert, 1968) that the retino-recipient pretectal thalamic structures (Lázár, 1969, Lázár, 1971, Lázár, 1989, Neary and Northcutt, 1983) via their anatomically verified connections to the optic tectum (Wilczynski and Northcutt, 1977) influence visual perception. Prey-recognition requires the intact pretectal thalamus, i.e. the lateral posterodorsal thalamic nucleus (Lpd) and the lateral posterior thalamic nucleus (P). Unilateral pretectal lesions led

Striatal influences on prey-catching behaviour

Prey stimuli are recognised by the processing of visual input in a parallel distributed interactive fashion that takes advantage of a retino-pretectal/tectal network which feeds the resulting information towards tegmental/bulbar/spinal structures. However, a toad's decision to respond to a prey object also depends on motivational factors (e.g. Guha et al., 1980, Laming and Cairns, 1998). Even a hungry toad is not necessarily attentive and therefore not responsive to prey. The brain modulates

The dopamine agonist apomorphine influences locomotory and ingestive components of prey-catching

In anurans, the retino-pretectal/tectal prey-catching release systems are controlled and modulated by striatal, limbic, pretectal, tegmental, preoptic/hypothalamic and solitary/reticular structures that contain dopaminergic cell bodies or fibres (González and Smeets, 1991, Marı́n et al., 1997d, Marı́n et al., 1997e). In common toads, systemic (intralymphatic) administration of the dopamine D2/D1 receptor agonist apomorphine (APO) modulates the orientational and consummatory components of

Behavioural studies

Habituation is defined as a decrement in the response activity with repeated stimulation (Thompson and Spencer, 1966, Groves and Thompson, 1970). If a prey dummy circles around the toad at a constant velocity and a constant distance to the toad, the prey-catching rate progressively decreases during this stimulus series until the toad remains unresponsive (Eikmanns, 1955). The toad's orienting activity reappears if (i) the same prey stimulus was withheld for a period of time [temporal recovery];

Concluding remarks

Unlike suggested at the beginning of the last century, visuomotor behaviours related to prey-catching and feeding in amphibians are not reflex-like, rather variable, flexible, and adaptable to the appropriate stimulus situations (e.g. see Anderson, 1993, Anderson and Nishikawa, 1993, Anderson and Nishikawa, 1996, Anderson and Nishikawa, 1997a, Anderson and Nishikawa, 1997b, Weerasuriya et al., 1994, Ewert et al., 1994a, Nishikawa and Gans, 1996, Valdez and Nishikawa, 1997, Gray et al., 1997,

General critical comments

Faced with the piece of reconstructed neural network shown in Fig. 1 — a simplification of the real one — our studies in brain function remind us on keyhole peeping, whereby the peephole is represented by the experimental technique. In fact, the limitations of our current knowledge are determined by the limitation of the applied experimental technique and the method of data evaluation. We extend our knowledge on a neural network by the application of different techniques that allow so-to-speak

Acknowledgements

We gratefully acknowledge the constructive comments on the manuscript by two anonymous referees. We thank Mrs K. Große-Mohr, Mrs C. Uthof, Mrs G. Kaschlaw and Mrs U. Reichert for technical assistance. The work was supported by the Deutsche Forschungsgemeinschaft (DFG), the Foundations' Fond for Research in Psychiatry, and the Bundesministerium für Bildung, Wissenschaft, Forschung und Technologie (BMBF) carried by the Deutsche Forschungsanstalt für Luft- und Raumfahrt (DLR) Project ‘SEKON’.

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