JOURNAL OF NEUROBIOLOGY, VOL. 6 , NO. 5, PP. 501-519
Physical and Physiological Properties of the Crayfish Antenna1 Flagellum ROBERT C. TAYLOR Department of Zoology, University of Georgia, Athens, Georgia 30602 SUMMARY
( 1 ) Mechanoreceptors in the crayfish antennae are divided into four functional categories: vibration (13%), bidirectional displacement (19%), unidirectional displacement (45%),and position (23%) receptors. The distribution of receptors along the length of the flagellum follows a logarithmic progression, decreasing from about 40% a t the base to less than 5% a t the tip. (2) Vibratory stimulation of the antennae was found to induce a traveling wave. Because of an impedance gradient along the length of the flagellum, the traveling wave moves most efficiently from base to tip. The wave was observed to travel a t an average velocity of 6.0 m/sec. ( 3 ) Large deflections of the tip are not uniformly transferred to the base, but decrease logarithmically. This is due to the existence of the impedance gradient. ( 4 ) Receptor output probability was found to be greatest when low frequencylhigh intensity stimulation was applied to the flagellar base. ( 5 ) Characteristics of large (2 cm) posterior-going deflections of the flagellar tip that are effective in producing response differences are displacement: ( a ) amplitude, ( b ) velocity, and (c) acceleration. INTRODUCTION
Although both the inhibitory effect produced by the supraesophageal ganglia (brain) on the lower ganglia (Schone, 1961 for review) and the output of the crayfish brain (Wiersma and Mill, 1965) have been known for some time, we still have very little knowledge about the major cephalic mechanoreceptors. Afferent inputs from these receptors terminate in the brain and are capable of controlling whole behavioral sequences (Taylor, in preparation). Integrative studies of the neuropiles that compose the brain must rest on a critical definition of the properties of these receptor organs. Consequently, a study was initiated dealing with the second antennae (antennae). This study discusses both the physical and physiological properties of the antenna1 flagellum and relates these to two forms of carefully specified input. Only two studies to date have presented physiological data from receptors in the decapod antennae (Taylor, 1967a,b; Hartman and Austin, 1972). The 501 01975 by John Wiley & Sons, Inc.
502
TAYLOR
first antennae (antennules) have been more intensively studied. Laverack (1964) studied the flagellar receptors and Wyse and Maynard (1965) described the joint receptors in the lobster antennule. Sandeman and Okaijima (1972) discussed the output from the statocyst of the crab Scylla. A t the behavioral level, the antennae appear to be active in orientation, social contacts, and defense. Many observations point to the importance of tactile stimuli in these behaviors. Generally, both pairs of antennae are involved (Cohen and Dijkgraff, 1961). In orientation, the antennae appear to be analogous to a blind man’s cane. Crayfish move their antennae up and down while pointing them in the direction that they are traveling, whether backwards, forwards, or sideways (Alverdes, 1930). This behavior probably plays a role in explaining the results of Gilhousen (1927), who found that crayfish trained to run a maze tended to turn too quickly when the antennae were amputated. Antenna1 input appears to increase in importance when vision is absent or drastically reduced. Blind, cave dwelling crayfish and deepsea lobsters each have extremely long antennae; lobsters have antennae up to four feet. In relation to the social contact category, blind crayfish can distinguish the anterior from the posterior of another crayfish by means of antennae alone (Bovbjerg, 1956). Bovbjerg also found that a rank order among four crayfish was maintained with either the eyes or the antennae, but not when both receptors were missing. In this case, the antennae provided the animal with enough information to distinguish between individual crayfish. The above results, as well as observations made in this laboratory, suggest that behaviorally effective mechanical stimulation of the antennae can be divided into two categories: (1) large posterior deflections (>0.1 cm) produced when an object is encountered, and also by water currents, edges, and the water surface; (2) relatively large amplitude vibrations (
Physical and Physiological Properties of the Crayfish Antenna1 Flagellum ROBERT C. TAYLOR Department of Zoology, University of Georgia, Athens, Georgia 30602 SUMMARY
( 1 ) Mechanoreceptors in the crayfish antennae are divided into four functional categories: vibration (13%), bidirectional displacement (19%), unidirectional displacement (45%),and position (23%) receptors. The distribution of receptors along the length of the flagellum follows a logarithmic progression, decreasing from about 40% a t the base to less than 5% a t the tip. (2) Vibratory stimulation of the antennae was found to induce a traveling wave. Because of an impedance gradient along the length of the flagellum, the traveling wave moves most efficiently from base to tip. The wave was observed to travel a t an average velocity of 6.0 m/sec. ( 3 ) Large deflections of the tip are not uniformly transferred to the base, but decrease logarithmically. This is due to the existence of the impedance gradient. ( 4 ) Receptor output probability was found to be greatest when low frequencylhigh intensity stimulation was applied to the flagellar base. ( 5 ) Characteristics of large (2 cm) posterior-going deflections of the flagellar tip that are effective in producing response differences are displacement: ( a ) amplitude, ( b ) velocity, and (c) acceleration. INTRODUCTION
Although both the inhibitory effect produced by the supraesophageal ganglia (brain) on the lower ganglia (Schone, 1961 for review) and the output of the crayfish brain (Wiersma and Mill, 1965) have been known for some time, we still have very little knowledge about the major cephalic mechanoreceptors. Afferent inputs from these receptors terminate in the brain and are capable of controlling whole behavioral sequences (Taylor, in preparation). Integrative studies of the neuropiles that compose the brain must rest on a critical definition of the properties of these receptor organs. Consequently, a study was initiated dealing with the second antennae (antennae). This study discusses both the physical and physiological properties of the antenna1 flagellum and relates these to two forms of carefully specified input. Only two studies to date have presented physiological data from receptors in the decapod antennae (Taylor, 1967a,b; Hartman and Austin, 1972). The 501 01975 by John Wiley & Sons, Inc.
502
TAYLOR
first antennae (antennules) have been more intensively studied. Laverack (1964) studied the flagellar receptors and Wyse and Maynard (1965) described the joint receptors in the lobster antennule. Sandeman and Okaijima (1972) discussed the output from the statocyst of the crab Scylla. A t the behavioral level, the antennae appear to be active in orientation, social contacts, and defense. Many observations point to the importance of tactile stimuli in these behaviors. Generally, both pairs of antennae are involved (Cohen and Dijkgraff, 1961). In orientation, the antennae appear to be analogous to a blind man’s cane. Crayfish move their antennae up and down while pointing them in the direction that they are traveling, whether backwards, forwards, or sideways (Alverdes, 1930). This behavior probably plays a role in explaining the results of Gilhousen (1927), who found that crayfish trained to run a maze tended to turn too quickly when the antennae were amputated. Antenna1 input appears to increase in importance when vision is absent or drastically reduced. Blind, cave dwelling crayfish and deepsea lobsters each have extremely long antennae; lobsters have antennae up to four feet. In relation to the social contact category, blind crayfish can distinguish the anterior from the posterior of another crayfish by means of antennae alone (Bovbjerg, 1956). Bovbjerg also found that a rank order among four crayfish was maintained with either the eyes or the antennae, but not when both receptors were missing. In this case, the antennae provided the animal with enough information to distinguish between individual crayfish. The above results, as well as observations made in this laboratory, suggest that behaviorally effective mechanical stimulation of the antennae can be divided into two categories: (1) large posterior deflections (>0.1 cm) produced when an object is encountered, and also by water currents, edges, and the water surface; (2) relatively large amplitude vibrations (
