Investigation of neurons involved in the analysis of gestalt prey features in the frogRana temporaria
In frogs,Rana temporaria, the activity of 63 single neurons-retinal ganglion cells (classes R 1, R2, and R3) and tectal neurons (classes T5(1), T5(2), T5(3) and T7) — were quantitatively investigated in response to different configurational moving stimuli of various sizes: (i) squares, (ii) stripes moving in direction of their long axis (worm configuration), and (iii) stripes moving perpendicular to the direction of their long axis (antiworm configuration). All stimuli were moved at constant visual angular velocity. Neuronal activity was evaluated using several methods.
The influence of stimulus area on the neuronal activity was investigated with square stimuli (Figs. 1–4, 6–10). Units were observed to respond optimally according to the different sizes of excitatory receptive fields. Retinal class R1 neurons (ERF=3.5° diam.) were best activated by ≈3° stimuli, class R2 (ERF =5.4°) by 3–4° stimuli and class R 3 (ERF=7.3°) by ≈8° stimuli. Tectal class T5(1) neurons (ERF=21.5°) were best activated by ≈8° stimuli, class T5(2) (ERF=17.6°) by ≈ 4° and class T5(3) (ERF=24.7°) by 8–16° stimuli. Class T 7 neurons (ERF=4.0°) were optimally activated in the range of 3–4°.
Effects of stimulus configuration on the neuronal activity were studied with stripes moving either in worm- or antiworm-configuration (Figs. 1–11). According to the receptive field organization in terms of a central ERF and a surrounding IRF, retinal ganglion cells exhibited different selective configurational sensitivity in distinct size ranges. If stripe stimuli were not longer than the diameter of the ERF, the antiworm configuration activated a ganglion cell more strongly than the worm configuration. This effect was most obvious in class R3 neurons. If stripes were longer than the ERF diameter then the worm was clearly preferred against the antiworm. This effect was strongest in R1 and R2 neurons. Tectal class T5(1) neurons showed almost no configurational sensitivity in the present context (Fig. 6); T5(2) neurons were more strongly activated by worm than by antiworm stimuli (Fig. 7), and T5 (3) neurons showed the reverse configurational preference (Fig. 9). Class T7 neurons exhibited worm preference only for stimuli longer than 8° (Fig. 10).
When the results inRana temporaria are compared with those previously obtained inBufo bufo (Figs. 11 and 12), it becomes evident that the investigated neurons of the visual system have similar response properties. However, the acuity of configurational selectivity in frog T5(2) neurons is not as sharp as that observed in corresponding tectal neurons in common toads.
In connection with the ‘command system concept’ — and in agreement with our earlier results — evidence is given that the outputs of several tectal neuron types, each forming acommand element, together constitute acommand system, which itself activates a specific motor pattern of the prey-catching sequence: orienting, approaching, fixating and snapping. Each motor command requires simultaneous activation of command elements subservingrecognition (stimulus classification) andlocalization (strategy of catching). We suggest that class T 5 (2) neurons are command elements with recognition properties, which are determinedby interaction of neuronal networks. The correspondingdecision-making process (prey/ nonprey)precedes the goal oriented behavioral response.
excitatory receptive field
inhibitory receptive field
caudal dorsal thalamus
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- Autrum H (1959) Das Fehlen unwillkürlicher Augenbewegungen beim Frosch. Naturwissenschaften 46:435Google Scholar
- Horchers H-W, Ewert J-P (1979) Correlation between behavioral and neuronal activities of toadsBufo bufo (L.) in response to moving configurational prey stimuli. Behav Proc 4:99–106Google Scholar
- Borchers H-W, Burghagen H, Ewert J-P (1978) Key stimuli of prey for toads (Bufo bufo L.): Configuration and movement patterns. J Comp Physiol 128:189–192Google Scholar
- Burghagen H (1979) Der Einfluß von figuralen, visuellen Mustern auf das Beutefangverhalten verschiedener Anuren. Ph. D. Thesis, Univ. KasselGoogle Scholar
- Corner C, Grobstein P (1978) Prey acquisition in atectal frogs. Brain Res 153:217–221Google Scholar
- Ewert J-P (1967) Aktivierung der Verhaltensfolge beim Beutefang der Erdkröte (Bufo bufo L.) durch elektrische Mittelhirnreizung. Z Vergl Physiol 54:455–481Google Scholar
- Ewert J-P (1968) Der Einfluß von Zwischenhirndefekten auf die Visuomotorik im Beutefang- und Fluchtverhalten der Erdkröte (Bufo bufo L.). Z Vergl Physiol 61:41–70Google Scholar
- Ewert J-P (1976) The visual system of the toad: Behavioral and physiological studies on a pattern recognition system. In: Fite KV (ed) The amphibian visual system. Academic Press, New York San Francisco London, pp 141–202Google Scholar
- Ewert J-P (1980) Neuroethology. An introduction to the neurophysiological fundamentals of behavior. Springer, Berlin Heidelberg New YorkGoogle Scholar
- Ewert J-P (1981) Tectal mechanisms underlying prey-catching and avoidance behaviors in toads. In: Vanegas H (ed) Neurology of the optic tectum. Plenum Press, New YorkGoogle Scholar
- Ewert J-P, Borchers H-W, Wietersheim A von (1978) Question of prey feature detectors in the toad'sBufo bufo (L.) visual system: A correlation analysis. J Comp Physiol 126:43–47Google Scholar
- Ewert J-P, Borchers H-W, Wietersheim A von (1979) Directional sensitivity, invariance and variability of tectal T 5 neurons in response to moving configurational stimuli in the toadBufo bufo (L.). J Comp Physiol 132:191–201Google Scholar
- Fite KV (1969) Single unit analysis of binocular neurons in the frog optic tectum. Exp Neurol 24:475–486Google Scholar
- Gaupp E, Ecker A, Wiedersheim R (1899) Anatomie des Frosches. Vieweg, BraunschweigGoogle Scholar
- George A (1975) Mikroelektrodenableitung einzelner Neurone im Tectum opticum vonR. esculenta. M. D. Thesis, BerlinGoogle Scholar
- Grüsser O-J, Grüsser-Cornehls U (1970a) Die Steuerung des Beutefang- und Fluchtverhaltens von Anuren durch verschiedene Nervenzellklassen im Tectum opticum. Pflügers Arch 319: R 149Google Scholar
- Grüsser O-J, Grüsser-Cornehls U (1970b) Die Neurophysiologie visuell gesteuerter Verhaltensweisen bei Anuren. Verhandl Dtsch Zool Ges 64:201–218Google Scholar
- Grüsser O-J, Grüsser-Cornehls U (1976) Neurophysiology of the anuran visual system. In: Llinás R, Precht W (eds) Frog neurobiology. Springer, Berlin Heidelberg New York, pp 298–385Google Scholar
- Himstedt W, Roth G (1980) Neuronal responses in the tectum opticum ofSalamandra to visual prey stimuli. J Comp Physiol 135:251–257Google Scholar
- Ingle D (1973) Disinhibition of tectal neurons by pretectal lesions in the frog. Science 180:422–424Google Scholar
- Ingle D (1975) Focal attention in the frog: Behavioral and physiological correlates. Science 188:1033–1035Google Scholar
- Ingle D (1980) Some effects of pretectum lesions on the frogs' detection of stationary objects. Behav Brain Res 1:139–163Google Scholar
- Kupferman J, Weiss KR (1978) The command neuron concept. Behav Brain Sci 1: 3–39Google Scholar
- Lázár G (1969) Efferent pathways of the optic tectum in the frog. Acta Biol Hung 20:171–183Google Scholar
- Lettvin JY, Maturana HR, McCulloch WS, Pitts WH (1959) What the frog's eye tells the frog's brain. Proc Inst Radio Eng NY 47:1940–1951Google Scholar
- Székely G, Lázár G (1976) Cellular and synaptic architecture of the optic tectum. In: Llinás R, Precht W (eds) Frog neurobiology. Springer, Berlin Heidelberg New York, pp 407–434Google Scholar
- Trachtenberg MC, Ingle D (1974) Thalamo-tectal projections in the frog. Brain Res 79:419–430Google Scholar
- Witpaard J (1976) Frog's vision. Nat. Thesis, LeidenGoogle Scholar