Tongue movements in the common boa (Constrictor constrictor)

Tongue movements in the common boa (Constrictor constrictor)

Anim. Behav., 1972,20, 373-382 TONGUE MOVEMENTS IN THE C O M M O N BOA (CONSTRICTOR CONSTRICTOR) BY PHILIP S. ULINSKI Loyola University School of ...

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Anim. Behav., 1972,20, 373-382

TONGUE MOVEMENTS

IN THE C O M M O N BOA

(CONSTRICTOR CONSTRICTOR) BY PHILIP S. ULINSKI

Loyola University School of Dentistry, Departments of Anatomy and Oral Biology, Maywood, Illinois, U.S.A. Abstract. Tongue movements were studied in Contsrictor constrictor by direct observation and by analysis of motion pictures. Vertical tongue movements consisted of an invariant sequence of protrusion, oscillation up and down, and retraction. Lateral deviation of the tongue occurred only in the company of vertical movements and was correlated with the direction of movement of the snake's head. Flick cluster duration varied from about 80 ms to about 1 s; variation in oscillation phase duration accounted for 69 per cent of the total variation. Oscillation phase duration varied linearly with the number of flicks in the flick cluster, suggesting that flick cluster duration is determined primarily by the number of oscillations which are carried out at a constant rate. One of the most obvious of a snake's attributes is its seemingly sinister habit of protruding its tongue and rapidly waving or 'flicking' it. In spite of the obtrusiveness of tongue flicking, no detailed study of snake tongue movements has been reported. Such a study is prompted by two considerations. First, the tongue is an important part of the ophidian adaptation to hunting and swallowing large prey (Gans 1961), for the snake's tongue does not participate in the manipulation of the prey and it is kept out of the way during swallowing by retraction into a specialized tongue sheath. The flicking movements performed by a snake's tongue are probably involved in collecting airborne particles, thereby giving the tongue a role in chemoreception. Secondly, the snake tongue, with its relatively small repertoire of movements, may serve as a 'model' system in which to study the neural control of vertebrate tongue movements. The intention of this study is to establish the overall pattern of tongue movements in the common boa or 'boa constrictor' (Constrictor constrictor) including: (a) a catalogue of boa tongue movements, (b) a determination of the sequences in which these movements can be performed, and (c) a description of the timing of these movements. This type of characterization falls short of establishing which movements a snake actually performs with its tongue in given circumstances. Factors such as temperature, humidity, lighting, hormone balance, nearness to shedding, time since feeding, and arousal state could conceivably influence the details of the tongue flicking pattern in an individual snake. No attempt was made to find out if the pattern of flicking in a given individual

varies from day to day. Some notice was taken of what kinds of tongue movements were executed by boas in a variety of situations, but these observations were ancillary to the study's main purpose. Although the mechanical aspects of snake tongue movements have not been described, several workers have considered various aspects of the biology of snake tongue flicking (Kahmann 1932, 1934; Wilde 1938; Noble & Claussen 1936; CoMes & Phelan 1958; Burghardt 1966, 1967, 1969, 1970; Sheffield, Law & Burghardt 1968; Burghardt & Hess 1968). The general consensus is that tongue flicking subserves a chemoreceptive role in prey detection. The exact sensory mechanisms involved are not understood, although the participation of the vomeronasal (or Jacobson's) organs has been implicated. The anatomy of the tongue has been described (Minot 1880; Sewertzoff 1929; Hershkowitz 1941) and the gross anatomy of the extrinsic muscles of the tongue is well known (see Langebartel 1968 for a general discussion and Gibson 1966 for C. constrictor). However, the functional anatomy of the tongue and its muscles and nerves has not been adequately treated. The present study was carried out by observing tongue flicking in specimens of C. constrictor and on motion pictures made of the same snakes. These observations were used to construct a general description of the pattern of boa tongue movements, to time the tongue's movements by a frame-by-frame analysis of the films, and to discover some of the factors which determine in which direction a snake points its tongue while flicking it. The observations will be reported in that order. 373

374

ANIMAL

BEHAVIOUR.,

A preliminary notice of this study has appeared (Ulinski 1971). Methods Seven specimens of C. constrictor (-----Boa constrictor) were used. They were purchased from C. P. Chase, Co., Miami and ranged in snout-vent length from 0.7 to 1-2 m. A single specimen of the eastern garter snake (Thamnophis sirtalis sirtalis) was used for comparative purposes. It was captured in Ingham County, Michigan. The snakes were maintained for some time before and after the observations in apparently good health. Tongue movements were recorded at twenty-four frames per s on 16-ram black and white, 4XR movie film. Tracings of the films were prepared on a Vanguard Motion Analyzer. Snakes were photographed in lateral, dorsal, and frontal views on separate occasions. Photographic sessions were carried out at room temperature which tended to be about 25~ Two investigators were involved in each session. One person operated the camera; the second person held the snake and encouraged it to protrude its tongue by rubbing the underside of its head and its nose. Since some individual snakes were more co-operative than others, and since some inter-individual differences in tongue movement patterns undoubtedly occur, it is possible that the sample of tongue flicks photographed in this way is biased in some regards. To control for this, an impression of the timing of boa tongue flicks was formed during the photographic sessions. This impression was compared with observations made on the same snakes while they were at liberty in a 1.3 x 2.8 x 0.6-m cage. The snakes were observed while exploring the cage immediately after being placed into the cage, while they were moving about after habituation, and during feeding sessions in which live mice were introduced into the cage. Observations were also made on C. constrictor in a large cage at the Lincoln Park Zoo. These observations indicated that the sample of tongue flicks photographed is probably representative of the movements which boas perform with their tongues under normal circumstances. Results Pattern of Tongue Movements Films of snake tongue flicking were studied to characterize the general pattern of movements which occur when a snake flicks its tongue. When the pattern of movements involved was

20,

2

understood, further corroborating observations of living snakes were made. Both sets of observations indicated that a very constant sequence of events is involved when a boa flicks its tongue. Tongue flicking begins by the protrusion of the tongue (Fig. 1). The tip of the tongue may be slightly upturned while the tongue is emerging from the mouth in some instances (see Fig. 3) but the body of the tongue is always protruded downwards from the mouth. The entire flicking process is called a 'flick cluster' here and the initial emergence of the tongue is called the protrusion phase of the cluster. When the tongue has been extended, it is moved up and down in a vertical plane one or more times. The number of movements vary (see below), but the pattern of the movements is always the same. The distance the tongue moves upwards is less than the distance it moves downwards, although the inertia of the tongue may bend the distal part upwards at the end of its upwards excursion just as the end of a rubber hose whips upwards if you shake the hose. Similarly, the tongue tip may bend downwards at the end of the tongue's downward excursion. This sequence of vertical movements is called the oscillation phase of the flick cluster. The tongue is pulled back into the mouth after the oscillation phase. This always happens following the down movement of an oscillation. As the tongue is re-entering the mouth, it is moving upwards, so inertia may again whip the tongue tip upwards as it reaches the lips. The withdrawal of the tongue after the oscillation phase is called the retraction phase of the flick cluster. The only deviation from this sequence of events which was observed is that occasionally the tongue may be brought back into the mouth without an oscillation phase immediately after the protrusion phase. When tongue flicking is viewed from above the snake (Fig. 2) it can be seen that the tongue movements do not necessarily occur in the snake's midsagittal plane; and, in fact, while a flick cluster is in progress the tongue can be pointed anywhere in front of the snake. Thus, the tongue may be directed below the horizontal plane or above it and it very often is directed laterally to one side or the other. The vertical movements which were described above take place in basically the same way regardless o f the tongue's direction. Similarly, you can extend your arm in any direction to shake someone's hand while moving your arm up and down vertically. Although a snake's tongue can be

ULINSKI: S N A K E T O N G U E F L I C K I N G START

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Fig. 1. Pattern of boa tongue movements in lateral view. Tracings of each frame in motion pictures of two complete flick clusters are illustrated. Successive pictures are about 42 ms apart in time. The ends of the protrusion phase (P), the oscillation phase (O), and the retraction phase (R) are indicated by vertical lines. The figures should be studied from left to right in each line.

placed lateral to the vertical plane, this movement is a fairly rigid one, and a snake was never seen to make the lateral tongue movements which mammals or lizards make when they are positioning food in their mouths (see Frazzetta 1962, Fig. 7, Abd-EI-Malek 1955) or licking their lips. Also, deviation from the midline in the horizontal plane occurs only during the course of vertical movements. A snake was never seen to protrude its tongue and then move it from side to side in the horizontal plane in the absence of vertical m.ovements. There is a fairly clear variation in the distance that a snake protrudes its tongue. The tongue is extended only a short distance during flick clusters of short duration and is fully extended during flick clusters of long duration. Once the tongue is extended during the protrusion phase, it appears that it is neither extended farther nor retracted until the start of the retraction phase. It was not possible to verify quantatively these appearances because the lateral deviations of the

tongue made it impossible to measure true tongue lengths on our films.

Timing of Vertical Tongue Movements The temporal aspects of vertical tongue movements were recorded from the films of boa tongue movements. Each flick cluster was given a number and was divided into constituent 'flicks'. One 'flick' is defined to be a movement of the snake's tongue which does not cross the horizontal plane. The division of a typical flick cluster into constituent flicks is illustrated in Fig. 3. The first flick is always identical to the protrusion phase and the last flick in a cluster is always identical to the retraction phase. The number of flicks in each flick cluster was determined by using this definition. The duration of each flick cluster and its phases were estimated by counting film frames. These data were used to determine: (a) the flick rate for each cluster, (b) the variation in the duration of the flick

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Fig. 2. Pattern of boa tongue movements in dorsal view. Tracings of each frame in motion pictures of three complete flick clusters are illustrated. Successive pictures are about 42 ms apart in time, The tongue shows a lateral deviation to the right (R) in the upper cluster, shows no significant deviation (S) in the middle cluster, and shows a lateral deviation to the left (L) in the lower cluster. The apparent shortening of the tongue is due to its elevation or lowering relative to the horizontal plane rather than to retraction.

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Fig. 3. Definition of a flick. The division of a flick cluster into eight constituent flicks is illustrated. A flick is defined as a tongue movement which does not cross the horizontal plane. Each flick is bracketed by vertical lines in this figure and is numbered at the end of the flick.

ULINSKI: SNAKE TONGUE FLICKING cluster, and (c) the mechanisms by which the duration of a flick cluster is controlled. Flick rate. The durations of ninety-eight flick clusters and the number of flicks in each cluster were determined for three individuals. The flick rate for each cluster was, thus, calculated. Figure 4A shows the distribution of these flick rates. A mean flick rate of 8.5 flicks per s was calculated. All of the boas which were observed had tongue flick rates which were consistent with this flick rate, but other kinds of snakes often had noticeably different flick rates. Figure 4B to E illustrates this by showing the distribution of flick rates for three individual C. constrictor and for a garter snake (T. s. sirtalis). The garter snake appears to have a faster flick rate than does C. constrictor, but a complete comparative study of flick rates was not undertaken. I.O lB. Ist

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of flick clusters for the ninety-eight clusters. The duration of an individual cluster ranged from two to twenty-five frames (or about 42 ms to about 1 s). The mean duration for the flick clusters was 12.8 frames or about 540 ms. Observations of boas in large cages indicated that boa flick cluster duration is related to the snake's current circumstances. A boa that is stalking a mouse, for example, will tend to remain almost motionless and, if it flicks its tongue at all, will limit itself to a few tongue flicks. Snakes that are moving about a large cage tend to demonstrate a steady sequence of short flick clusters. However, snakes that are being handled or are subjected to novel stimuli tend to flick their tongues for the relatively longest period of time. Since the histogram in Fig. 5 was constructed from data obtained from hand held snakes the mean duration is probably biased towards a longer flick duration. However, there is no reason to doubt that the range of durations represented reflect the physiological range of flick cluster durations that the neuromuscular system of the b o a ' s tongue can produce.

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Fig. 4. Flick rate in C. constrictor and in Thamnophis s. sirtalis. A. A histogram of tongue flick rates in three individuals of C. constrictor. A total of ninety-eight flick clusters were sampled. B, C and D: Histograms of tongue flick rates prepared from samples of the data in (A) to illustrate the extent of inter-individual variation in flick rate. E: A histogram of flick rate in one individual of Thamnophis s. sirtalis to illustrate the possibility of interspecific variation in flick rate. Flick cluster duration. Although a snake may be flicking its tongue at a rate of 8-5 flicks per s, the flick cluster may not last for an entire second. Figure 5 shows the distribution of the durations

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histogram of the duration of ninety-eight flick clusters in three boas. The mean and the standard error of the mean of the data is also presented. Control of cluster duration, There are three basic ways in which the duration of the flick cluster could be lengthened. First, the durations of the protraction or retraction phases could be lengthened by decreasing the rate of tongue movement. Second, the duration of the oscillation phase could be lengthened by decreasing the rate at which a constant number of flicks are performed. Or, third, the oscillation phase could be lengthened by increasing the number of flicks which are executed at a constant rate.

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Fig. 6. Durations of protrusion, oscillation, and retraction phases of C. constrictor. Histograms of the three flick cluster phases are presented based on ninety-eight flick clusters in three individuals. The means and the standard errors of the means are also presented. Table I. Variance of the Duration of Flick Cluster Phases and of Total Flick Duration

Per cent of total flick cluster Variance (frames2) variance Protrusion phase Oscillation phase Retraction phase Sum Total flick cluster

1'62 12.08 1.84 15.54 17.70

9"2 68"2 10.4 87.8 100.0

To assess these alternatives, the range in the duration of each of the three flick cluster phases was first calculated (Fig. 6). In the sample of ninety-eight clusters, the protrusion phase varied in duration from one to four frames (40 to 170 ms), the oscillation phase varied in duration from zero to sixteen frames (zero to 670 ms), and the retraction phase varied in duration from zero to six frames (zero to 250 ms). The variance of the duration of each phase was calculated (see Table I). Since the distributions in Fig. 6 are not perfectly Gaussian, the sum of the variances of the three phase distributions is not exactly equal to the variance of the total flick cluster distribution of Fig. 5. However, the protrusion phase and the retraction phase together account for only 19.6 per cent of the total variance. Thus, the duration of the oscillation phase seems to be the major factor in determining the duration of the total flick cluster. Consideration of the second and third choices requires a determination of the relation between the duration of each phase of a cluster to the

number of flicks in the cluster. These two variables were plotted for each of the ninety-eight clusters for each phase (Fig. 7). Linear regression curves were then calculated for the data in each phase. The data for the protrusion phase were found to be correlated with the regression curve by a product-moment correlation coefficient of r = 0.74. The slope of the regression curve was 0-04 frames per flick, which was not significantly different from zero (t = 0.58, d r = 94, 0-70 < P < 0.75). This suggests that the duration of the protrusion phase does not vary systematically with the number of flicks in the cluster. The data for the oscillation phase correlated with the regression line for that phase with a coefficient of r = 0-88. The slope of the regression line was 1.84 frames per flick or about 60 ms per flick. This suggests that the flick rate is constant throughout the oscillation phase and that the duration of the phase is determined by the number of flicks performed. The data for the retraction phase did not correlate well with the regression curve, but it seems d e a r from Fig. 7 that the duration of the phase is longer when a larger number of flicks have preceded the retraction. Direction of Tongue During Flick Cluster

The observations on freely moving snakes reported above indicated that lateral deviations of the tongue are often superimposed on the vertical movements during a flick cluster. Thus, the frequency with which lateral deviations of the tongue occurred to the right or to the left was studied to determine whether or not these lateral deviations occur randomly. Snakes were placed

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Fig. 7. Relation of flick duster phase duration to the number of flicks in the cluster. A: The relation of the total flick cluster duration to the number of constituent flicks is plotted as open circles. The duration of the protrusion phase (P) is plotted as a function of the number of flicks in the total flick cluster (F) in the filled circles. The linear regression curve is indicated. B: The duration of the oscillation phase (S) is plotted as a function of the number of flicks in the total flick cluster (F), and the linear regression curve is indicated. C: The duration of the retraction phase is plotted as a function of the number of flicks in the total flick cluster. Ninety-eight flick clusters were used to prepare each graph, but only one data point was placed at each coordinate point even if several data points fell at those coordinates. Table II. Number of Flick Clusters Showing Deviations or No Deviations

Tongue direction Snake

L

S

R

1 2 3 Total

119 79 179 377

121 49 36 206

168 96 155 419

L = left lateral deviation; R = right lateral deviation; S = no lateral deviation.

individually on the large, tile floor of a laboratory and allowed to move freely. An observer stood behind the snake and recorded for each flick cluster whether the tongue deviated to the left (L), did not deviate to either side (S), or deviated to the right (R). This was done with three individuals for a total of 1002 flick clusters. Since the snakes and their tongues were moving, errors of judgment undoubtedly occurred in this procedure. It was usually easy to separate deviations to the left from those to the right, but it was often difficult to be certain that no deviation was occurring in an individual flick cluster. Table II displays the number of flick dusters showing lateral deviations or showing no deviations in this series of observations. Flick

clusters showing deviations, to the left or to the right, occurred about three times as often as did flick clusters showing no deviations, but deviations to one side did not occur statistically more often than to the other side (~2 = 2.21; 0.10 < P < 0.20). Examination of the record of these observations suggested that the sequence of deviations is non-random in that deviation to the same side tended to occur in several successive flick clusters; Table III illustrates this. Further observations on freely moving snakes indicated that a correlation may exist between the direction of the tongue's deviations and the direction in which the snake's head is moving. While a snake was moving about on the tile floor of the laboratory he spent most of the time with the back part of his body fixed and making wide sweeping, exploratory arcs with his head. The second most frequent motion was a rectilinear locomotion (Lissmann 1950) which the snake performed with his body almost completely straight. Few lateral tongue deviations occurred when a snake was moving straight ahead, and his tongue deviated in the same direction in which his head was moving during the sequence of flick clusters performed while his head was moving in an arc. To verify this observation,

380

ANIMAL

BEHAVIOUR,

20,

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Table III, Tongue Direction in One Hundred Successive Flick Clusters in a Free Ranging Boa

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L = Left lateral deviation, R = Right lateral deviation, S = No lateral deviation. The record should be read from left to right. recorded.) These d a t a indicate a strong correlation between direction o f head m o v e m e n t a n d direction o f tongue d e v i a t i o n (see Fig. 8). This correlation is reflected quantitatively in a coefficient o f contingency o f C = 0.79 for the d a t a in Fig. 8.

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Fig. 8. Relation of the direction of tongue deviation to the direction of head movement. The direction in which the heads of three individuals were moving (left, right or straight ahead) and the direction of the tongue's lateral deviation (left, right or no deviation) were scored for a total of 243 flick clusters. The number of times which each of the nine possible scores occurred is entered in the ceils of the matrix. The coefficient of contingency (C) and chi-square are indicated; the associated probability, P, was !ess than 0.001. The head figures illustrate the two types of lateral deviation. R=right; L=left; S=straight ahead or no edviation. records were m a d e o f b o t h the direction o f tongue deviation a n d the direction o f h e a d m o v e m e n t (right, left o r straight ahead) on three snakes. F l i c k clusters were scored in this case only if the snake was m o v i n g a n d only if b o t h directions could be clearly discerned. Observations were m a d e on three individuals for a total o f 243 flick clusters. (A great m a n y a d d i tional flick clusters were observed b u t n o t

Only f o u r basic tongue m o v e m e n t s were o b s e r v e d in C. constrictor (Fig. 9); the tongue was p r o t r u d e d (P), it was elevated (E) in a vertical plane, it was lowered in a vertical plane (L), a n d it was retracted (R). N o i n d e p e n d e n t lateral m o v e m e n t s o f the tongue were seen a n d no significant t u r n i n g o f the tongue on its l o n g i t u d i n a l axis to face laterally was seen. T h e

Fig. 9. Diagrammatic summary of the pattern of boa tongue movements. The tongue is first protruded (P). It is then successively elevated (E) and lowered (L) a variable number of times. Finally, it is retracted (R) from below the horizontal plane. latter m o v e m e n t forms an i m p o r t a n t p a r t o f the t o n g u e ' s m a s t i c a t o r y m o t i o n s in h u m a n s ( A b d E1-Malek 1955) a n d has also been r e p o r t e d in cats ( M o r i m o t o , K a t o & K a w a m u r a 1966) a n d in dogs (Bennett & H u t c h i n s o n 1946) in experim e n t a l situations. M o v e m e n t s in the b o a tongue were seen to be assembled into only one basic serial p a t t e r n which can be symbolized as P(EL)NR N = 0, 1, 2 . . . . . where N m e a n s the sequence in parentheses c a n be r e p e a t e d a different integral n u m b e r o f times in different flick clusters or m a y be absent f r o m

ULINSKI: SNAKE TONGUE FLICKING the sequence (N = 0). This limitation of the tongue's motor activities to a small repertoire of movements which can be assembled into a single serial pattern is clearly correlated with the evolutionary change in the tongue from a prey positioning organ (Gans 1961) to a chemoreceptive organ which does not participate in prey positioning, in mastication, or in deglutition during the snake-lizard transition. No previous detailed description of snake tongue movements comparable to that in this paper has been published and no earlier author seems to have given a definition of a 'flick', so there is no set of data which can be legitimately compared to the present data. Burghardt (1969) used counts of tongue flicks as part of an index to test the abilities of several species of garter snakes to detect prey extracts. Judging from his values, he used the word 'flick' to denote the sequence of events which have been called a 'flick cluster' here. The present description of boa tongue movements is probably basically representative of tongue movements in other snakes, but variations in timing certainly are present between species. Also, some species are said to be able to protrude their tongues without oscillating them (Parker 1963, p. 89), possibly as a protective warning device. An extension of our studies to other snakes is in order, and it would be particularly interesting to have a description of tongue movements in lizards such as varanids or teiids which have a snake-like bifid tongue. Control of Oscillation Phase Duration Although there is some variation in the duration of the protrusion and retraction phases, the major variation in flick cluster length is caused by the addition of flicks at a constant rate in the oscillation phase. Also, a definite correlation exists between environmental circumstances and flick cluster duration in C. constrictor. However, a comprehensive study of the environmental influences on tongue flicking and the effective stimuli which directly relate to tongue behaviours was not undertaken. Future studies on these subjects are indicated. Little is known about the neural control of flick cluster duration. It is plausible that visual, auditory, somatic and visceral stimuli could influence the tongue's neuromuscular system by a variety of routes, but so little is known about snake neuroanatomy that few positive statements are possible. One interesting possibility is suggested by Wilde's (1938) observation that

381

severance of the vomeronasal nerves in T. s.

sirtalis caused a statistically significant reduction in the number of tongue 'extensions' elicited by the presentation of olfactory stimuli. It is thought that the tongue aids in carrying substances to the vomeronasal organs (Wilde 1938). These organs are connected to the accessory olfactory bulbs, and neurons from the bulbs send processes to synapse on cells (Heimer 1969; the tegu lizard, Tupinambis teguixin) within the highly elaborated 'nucleus sphericus' (Goldby & Gamble 1957) which is unique to snakes and lizards (Northcutt 1967). The termination of the axons of nucleus sphericus cells is not known, but it is tempting to suggest that they influence the hypoglossal motoneurons in some way, closing the loop of a feedback system which mediates flick cluster frequency or duration. Microelectrode recordings from hypoglossal motoneurons while stimulating the vomeronasal nerves are needed to test this hypothesis. Lateral Deviation of the Tongue In free-ranging snakes the direction in which the tongue points during a flick cluster is correlated to the direction in which the snake's head is moving. Since the tongue's inertia will tend to point the tongue in a direction opposite to the head's movement, this correlation indicates that the tongue's lateral deviation is under active muscular control. The correlation does not prove a causal relation between head movement and tongue deviation. However, a possible mechanism for such a relation is suggested by Ebbesson's (1969) report that fibres running in the lateral funiculus of the spinal cord in snakes (C. constrictor) which had previously undergone hemicordotomies could be traced in Nauta preparations through the ipsilateral hypoglossal nucleus into a small-celled nucleus lying just medial to the hypoglossal nucleus. If these fibres terminate directly or indirectly on hypoglossal motoneurons, this pathway could provide a mechanism which gives hypoglossal motoneurons ipsilateral to contracting spinal musculature an excitatory bias. Microelectrode recordings from hypoglossal motoneurons in preparations in which spinal nerves are stimulated are needed to examine this hypothesis. The existence of such a system would not rule out other influences on tongue deviations. Acknowledgments This work was supported by special funds from Oberlin College and from Loyola University

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School of Dentistry. William Jungers and John Blickenstaff provided photographic assistance. Mary Rita Perkins typed the manuscript. Dr Carl Gans, Dr Robert Schmidt and Dr Warren Walker read the manuscript and made very valuable criticisms. REFERENCES Abd-E1-Malek, S. (1955). The part played by the tongue in mastication and deglutition. J. Anat. (Lond.), 89, 250-254. Bennett, G. A. & Hutchinson, R. C. (1946). Experimental studies on the movement of the mammalian tongue. II. The protrusion mechanism of the tongue (dog). Anat. Rec., 94, 57-83. Burghardt, G. M. (1966). Stimulus control of the prey attack response in naive garter snakes. Psychonom. Sci., 4, 37-38. Burghardt, G. M. (1967). Chemical preference studies on newborn snakes of three sympatric species of Natrix. Copeia, 1967, 732-737. Burghardt, G. M. (1969). Comparative prey-attack studies in newborn snakes of the genus Thamnophis Behaviour, 33, 77-114. Burghardt, G. M. (1970). Intraspecific geographical variation in chemical food cue preferences of newborn garter snakes (Thamnophis sirtalis). Behaviour, 36, 246-257. Burghardt, G. M. & Hess, E. H. (1968). Factors influencing the chemical release of prey attack in newborn snakes. J. comp. physiol. Psych., 66, 289-295. Cowles, R. B. & Phelan, R. L. (1958). Olfaction in rattlesnakes. Copeia, 1958, 77-83. Ebbesson, S. O. E. (1969). Brain stem afferents from the spinal chord in a sample of reptilian and amphibian species. Ann. N. Y. Acad. Sci., 167(1), 80-101. Frazzetta, T. H. (1962). A functional consideration of cranial kinesis in lizards. J. Morph., 111, 287-319. Gans, C. (1961). The feeding mechanisms of snakes and its possible evolution. Am. Zool., 1, 217-227. Gibson, F. W. (1966). Head muscles of Boa constrictor. Zoologica, 51, 29-48. Goldby, F. & Gamble, H. J. (1957). The reptilian cerebral hemispheres. Biol. Rev., 32, 382--420.

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