Use of Innate Behaviors to Evaluate Sensory Function in the Dog

Advances in Companion Animal Behavior

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Use of Innate Behaviors to Evaluate Sensory Function in the Dog L.]. Myers, DVM, MS, PhD*

The evaluation of sensory function has been an orphan in the field of veterinary medicine. This is probably because of the scarcity and expense of techniques available and known to the practicing veterinarian. Recent research has developed new techniques that are relatively inexpensive and easy to use. Few people doubt the importance of sensory function to the animals under our care. Although introspection and anthropomorphosis are not the best tools for science, they do suggest that the welfare of a dog, cat, horse, or other pet, is diminished significantly by the impairment of any of its senses. It is doubtful that the impact of impairment on a domestic animal's welfare is equivalent to that of a human's, because the sensory capacity as well as cognitive function are different for different species ..For example, the loss of the sense of smell is much more important to a dog than the corresponding loss is to a person,. because the dog's sense of smell is much more acute than a human's and is more obviously involved in the day to day behavior of the dog. On the other hand, loss of vision is more significant to a human than to a dog. Furthermore, the sensory function of some domestic animals is quite important to humans. The sensory capacity of an animal must be adequate to its function. The visual capacity of a racehorse is vital to its function on the racetrack just as the olfactory capacity of cow is vital to its social and, probably, its breeding behavior. 4

MAJOR METHODS OF EVALUATING SENSORY FUNCTION There are a number of major categories of techniques to evaluate sensory function in animals. These include (1) operant conditioning, (2) *Director, Institute for Biological Detection Systems, and Assistant Professor, Department of Physiology and Pharmacology, Auburn University College of Veterinary Medicine, Auburn, Alabama Veterinary Clinics of North America: Small Animal Practice-Yo!. 21, No. 2, March 1991

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classical conditioning, (3) electrophysiologic techniques, and (4) innate behavioral techniques. Each has unique advantages and disadvantages. Operant Conditioning Operant conditioning techniques comprise the standard by which the other techniques for evaluating sensory function are judged. They are versatile and accurate and may be used to evaluate the capabilities of discrimination of an animal. The body of literature surrounding these techniques is vast. Operant conditioning techniques, however, will never have great use in veterinary practice. Disadvantages of these techniques are the time and expense of training an animal to an adequate level (criterion) of correct response to evaluate sensory function. It also is impractical to condition an animal to perform a sensory task when a clinical condition is present that might prevent it from responding appropriately. Classical Conditioning Classical conditioning techniques are similar to operant conditioning techniques in that a training period is required, but the response is autonomic rather than operant. The most famous example, of course, is the conditioning of a dog to salivate at the sound of a bell associated with presentation of food. The disadvantages of these techniques are the same as for operant conditioning. Electrophysiologic Techniques Electrophysiologic techniques for evaluation of sensory function have been important methods for the veterinary· profession. They have the advantage of being highly objective, particularly with most of the evoked responses, and they are well accepted by the profession. For example, the brainstem auditory-evoked response (BAER) is an excellent technique for evaluation of auditory brainstem function, as is the electroretinogram (ERG) for retinal function. 1• 17 These techniques, however, have certain disadvantages that suggest the need for alternative methods of evaluating sensory function. The evoked responses normally measure the activity of only a portion of the nervous system associated with a sensory modality. Most of these techniques require anesthesia of the animal, and all require relatively expensive equipment. Innate Behavioral Techniques Innate behavioral techniques for detailed sensory evaluation have not been used often by veterinarians. This may be because of the lack of published research on the topic in the veterinary literature until recent years. These techniques have been in formal use, however, since the initiation of the neurologic examination, and they were used for sensory evaluation of animals nearly a century ago. 18

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Innate behavioral methods depend upon an observable behavior that can be evoked reliably by a stimulus without the requirement of learning. The best known examples of such behaviors are simple spinal reflexes, such as the patellar reflex. Other examples abound, including not only relatively simple reflexes but also complex behaviors such as the freeze response of young ungulates and the pecking response of young birds. 14 Use of innate behaviors to evaluate sensory function offers a variety of advantages. In most cases, they take little time to perform, and the equipment and supplies required are inexpensive. These techniques are objective, accurate, and are intuitively understandable by clients. GENERAL PRINCIPLES OF INNATE BEHAVIORAL METHODS Stimulus Control One of the foremost principles in sensory evaluation of any type is that the stimulus must be controlled carefully. The specific methods of stimulus presentation are discussed in the descriptions to follow. The principle applies, however, not only to the stimulus being purposely presented but also to the extraneous stimuli in the testing environment. For example, it is futile to evaluate visual acuity in a conscious animal with other visual stimuli in the test area beside that being presented; but it also is inappropriate to allow loud sounds in the test area. The environment for sensory evaluation is never stimulus-free. There are always extraneous sounds, tactile stimuli, sights, odors, and tastes. The best the examiner can accomplish is to produce a stimulus-neutral environment: that is, one in which the extraneous stimuli are at a low and relatively constant level. In the author's laboratory, animals are blindfolded for tests oth~r than visual acuity, sound is masked by white noise, odors are controlled (no smoking, perfume, or cologne are allowed, and baking soda is placed in bags as an odor absorbent), temperature is controlled, and animals are allowed a minimum of5 minutes to acclimate to the environment before being tested. This sort of stimulus-neutral environment is simple to create and maintain. Adaptation of Response Caution must be exercised to avoid repetition of stimulus presentation to the extent that adaptation of response alters estimates of sensory function. Physiologic adaptation is the phenomenon associated with repetitive or constant stimulus presentation that results in loss of responsiveness of the physiologic system to the stimulus. 12 This is noted particularly in the olfactory and gustatory systems. It has been ascertained that stimuli for evaluation of these systems must be presented in ascending order, from the weakest to the strongest, because adaptation occurs rapidly, preventing responses evoked by the weaker stimuli. 18• 20

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Objectivity of Evaluation

Innate behavioral techniques provide an objective evaluation of sensory capacity when used properly. In the author's laboratory, studies of interobserver variability for behavioral olfactometry and optokinetic visual acuity evaluation showed that trained observers agreed in 100% of the evaluations. 19 Personnel must be trained to identify the innate behavioral pattern with certainty and to be conservative in interpretation of the results. The behavior can be videotaped to provide a record for later interpretation or for archival purposes. Limits of Techniques

Innate behavioral techniques are not without their inherent limits. The aim of the techniques described in this article is to evaluate sensory function, but each technique depends on intact neural integrative centers for the behavior and upon the integrity of the associated motor component. The state of awareness of the animal may also alter results; for example, olfactory evaluation of a sleeping or obviously agitated dog is not valid. Although not a limitation of technique, excessive interpretation of results is a danger associated with sensory evaluation. The innate behavioral techniques do not determine cognitive abilities such as scent discrimination nor do they predict performance such as the level at which a dog will perform in a field trial.

OLFACTORY SYSTEM

Although olfactory abnormalities have been the source of client complaints among the owners of field-trial dogs, the diagnosis of olfactory problems rarely has been made by veterinary practitioners. This is illustrated by the responses to a questionnaire by owners of hunting dogs indicating that 85% have at some time experienced what they considered to be olfactory problems with their animals. 15 The Veterinary Neurologic Examination

Simple presence or absence of olfactory function has been diagnosed by an innate motor response (sniff or directed approach or avoidance) evoked by a strongly odoriferous substance placed near a dog's nose. 25 This test has been used in the complete veterinary neurologic examination for some years. Unfortunately, it often has been misapplied. Strong trigeminal stimulants such as ammonia or vinegar test the integrity of the intranasal trigeminal rather than olfactory nerve function. They also may cause stimulation of the trigeminal receptors of mucous membranes other than the intranasal respiratory and olfactory mucosa, causing a behavioral response that might be confused with an olfactory response. The author

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recommends eugenol, which has been demonstrated in humans to be a relatively pure olfactory nerve stimulant. 6 The ability of the dog to see the odor stimulus presented results in false-positive responses. Therefore, animals should be blindfolded during olfactory evaluation. The author has observed dogs made anosmic by zinc sulfate lavage respond when odorless tubes containing propylene glycol were placed near the nose. These dogs did not respond to the presentation of tubes containing high concentrations of highly odoriferous eugenol when blindfolded. Behavioral Olfactometry Electroencephalographic olfactometry (EEGO) and behavioral olfactometry were described some years ago with normative data provided for benzaldehyde and eugenol. 20 These techniques normally are performed simultaneously in the author's laboratory. Both techniques are effective in determining the threshold of response to a variety of odors for normal and abnormal dogs. EEGO has been demonstrated to be slightly more sensitive and precise than behavioral olfactometry, but behavioral olfactometry alone also is effective. The odorant selected should be serially diluted in log increments in pharmaceutic-grade propylene glycol in 16 increments. One mL of eac}_l dilution should be placed in a 12 X 75 mm borosilicate tube and sealed. For an odorless blank, 1 mL of propylene glycoJ should be placed in a tube and sealed. Care should be taken that no trace of the odoriferous substances remains on the exterior of the containers. The dog to be tested should .be placed in a right lateral recumbent position in a stimulus-neutral area, blindfolded, and calmed. Each dilution sample should be opened and placed 2 em ventral to the tip of the nose of the animal to be tested, beginning with the odorless blank (propylene glycol) stimulus, followed by presentation of the most dilute sample (1015), and continuing with each increasing concentration until response is observed. Each dilution should be presented for 10 seconds, withdrawn for 15 seconds, and then followed by the next concentration. A positive behavioral olfactometry response is determined by a typical behavioral pattern consisting of one or more of the following: sniffing, licking the nose, or movement of the head toward or away from the odor source. The threshold was determined for each type of olfactometry as the least concentrated dilution that evoked a recognizable response. 20 The normal values for clinically normal, adult dogs of various breeds are provided in Table 1. Conditions Associated with Dysosmia The use of behavioral olfactometry in conjunction with EEGO has demonstrated that a substantial number of conditions cause or are associated with olfactory dysfunction in the dog. These conditions include canine

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Table 1. Normative Values of Innate Behavioral Techniques for Dogs

TECHNIQUE

STIMULUS

THRESHOLD

Behavioral olfactometry

eugenol benzaldehyde sucrose vertical 1000Hz

-12

Behavioral gustometry Optokinetic response Preyer's reflex

-II -ll

5.4' Not applicable

NORMAL RANGE (LOG 10 OF GRADE SOLUTION)

-16 to -8 -14to -6 -15 to -7 5. 04 to 5. 75' arc Not applicable

distemper, canine parainfluenza, hypothyroidism, iatrogenic Cushing's disease, diabetes mellitus, seizure disorders, and head trauma7· 21 • 23 (Myers L, unpublished data). Other conditions are suspected to cause olfactory dysfunction but have not been fully evaluated. These include aspergilliosis, allergic rhinitis, inhalation of various toxins, and hepatoencephalopathy.

GUSTATORY SYSTEM The clinical significance of the sense of taste in domestic animals has not been explored. The standard veterinary neurologic examination does not include a method by which taste function can be evaluated, and disorders of taste function (dysgeusias) are not readily observable by clients. A substantial number of cases of dysgeusia, however, have been reported in human medicine. 26 This leads one to the conclusion that the sense of taste may have clinical importance in domestic animals. It ·is expected that dysgeusias may be sequelae to a variety of other conditions and may manifest themselves as eating or other behavioral disorders. 26 Palatability Tests A simple method that provides an index of taste function in a domestic animal is the p~latability test: 9 • 23 This test, however, primarily is a measure of taste preference rather than a measure of gustatory function .. The simplest tests use a two-choice system in which two dishes containing food (or fluid) are provided free-choice to the animal to be evaluated. The amount consumed, the frequency of consumption, and the duration of consumption are measured during a set period to determine the preference of the animal. This can serve as an index of taste function if the relative preferences of the food items are known for healthy animals. Behavioral Gustometry Behavioral gustometry is a method that primarily is aimed at evaluation of taste sensory function. This technique has as its basis the innate response to a novel flavor sensation: the act of licking. The innate behavior has been studied by a number of investigators. Scwartz and Grill27 used ascending

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series of stimuli applied by means of intraoral fistulae in rats to evaluate behavioral response. One mL was applied in 1 minute. For sucrose, the higher the concentration, the greater the number of ingestive response components seen. Grill 12 applied ascending series of 50 J.LL of taste stimuli by means of intraoral fistulae in rats. It was found that 3 X I0- 2 mol/L sucrose evoked a full stereotypic behavioral pattern in 50% of the trials. Ganchrow et al 11 found orofacial expression of neonatal humans to be innate and effective in estimation of hedonic quality and intensity of a variety of taste stimuli including sucrose. The innate behaviors of licking and other alterations of orofacial expression also are evoked, however, by tactile stimulation of the tongue and buccal cavity. 12 Therefore, the primary problem of technique development was stimulus control. Most veterinary practitioners have observed the licking, and sometimes, gagging, that an animal exhibits a few seconds after an intravenous chloramphenicol injection. This is an innate behavioral response to intravenous taste. Bradley and Mistretta2 demonstrated that intravenously applied sodium saccharin coupled with an adverse stimulus is capable of producing taste aversion to oral saccharin in rats, implying that the sensation resulting from intravenous application is similar to that resulting from oral application. For intravenous application, stimulus solutions should be prepared in a Ringer's solution in log dilutions ranging 'from IQ- 6 to IQ- 12 molar. concentration of the taste compound. The solutions should be at room temperature when used. The author's laboratory has used sweet compounds (glucose, fructose, sucrose, and saccharine) and a bitter compound (quinine hydrochloride). Salt and sour compounds have not been used because of the potential for adverse osmolarity and pH effects upon the animal. Dogs should .be tested no less than 2 hours after feeding to reduce the possible effects of a recent meal on taste thresholds. A catheter is placed in the cephalic vein of each dog immediately before its use in the procedure. The dog is placed in right lateral recumbency on a cushioned table and blindfolded. The area should be stimulus neutral. A syringe pump is used to deliver 5 mL of solution per minute intravenously for 2 minutes per dilution. Solutions are delivered in the following order: Ringer's, IQ- 12 mol/L taste substance in carrier (Ringer's), w-u mol/L taste substance in carrier, and so on in ascending order until the threshold is reached as indicated by behavioral response or until a concentration of IQ- 6 mol/Lis reached. This maximum concentration (l0- 6 mol/L) was selected on the bases of mean thresholds for response observed, the concern over effects of osmolarity, and the temporal effects of mild restraint on the behavior of the dog. The gustatory response is defined as licking or swallowing by the dog in association with the overt stimulus. The Ringer's solution frequently evokes a gustatory response. This is probably a result of the activation of a

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salt-taste sensation, because the salt content of Ringer's does not match precisely the osmolarity and salinity of the animal. By applying Ringer's solution. alone, one sees gustatory response, which extinguishes rapidly. The response is not evoked by additional Ringer's solution. Thus, the response following the initial exposure to Ringer's solution is to the only change in composition, the addition of taste substance. Although behavioral gustometry measures taste function and is reliable, the thresholds obtained by the slow infusion technique are much lower than those obtained by a rapid infusion. No explanation is available for this phenomenon. VISUAL SYSTEM

The iJUportance of vision to the dog is obvious. Vision certainly has important effects on the behavior of dogs and on their performance and welfare. Dogs have been shown to have functional or anatomic visual deficits because of a variety of causes. Heritable conditions that alter visual function without obvious physical signs are common in dogs. Only a few methods customarily are used to evaluate the visual system of the dog. These include the menace response, the opthalmologic examination, ERGs, and the visual-evoked response (VER). 18 The menace response measures the presence or absence of visual capability. The opthalmologic examination provides anatomic information. The VER and ERG provide some functional information, but they are relatively expensive and inconvenient, and the anesthesia normally required places the dog at risk. Two innate behavioral techniques offer potentiitl functional measures of visual acuity in the dog. The preferred looking technique has not yet been developed for the dog, and it is presented as a potential technique. The other technique, optokinetic nystagmus (OKN), has been recently developed and is extremely reliable. 8 Preferred Looking A technique that has been successful in determining visual acuity in cats is the preferred looking phenomenon. This phenomenon, which is exhibited by cats and human infants, involves the preference of test subjects to look at figures exhibiting irregular contour. A set of curves is preferred over a set of straight lines. This has been adapted to techniques to evaluate visual acuity. 27 Optokinetic Nystagmus Technique The dog possesses an optokinetic reflex, called OKN, which is evoked by visual stimuli in motion. The anatomic and physiologic determinants of this reflex are described elsewhere. 5 The motor component of the reflex is movement of the eyes and head to follow the direction of motion of the

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visual stimulus. This reflex may be used to determine normal visual acuity for regular visual patterns in motion as a diagnostic method for visual deficits in the dog. OKN has been used effectively to evaluate visual acuity of human infants and cats. 10• 16 A commercial unit is used to present the stimulus for the optokinetic method for determining visual acuity. This unit generates precise, highcontrast grids of vertical bars in motion. The dog is restrained in a sling or similar restraint system with the cornea of the eye(s) to be tested 30 em from the stimulus unit. A drape is placed so that any movement in the surrounding area is not visible to the dog. The OKN response can be observed directly by leaving a small opening in the drape arrangement directly over the eyes of the dog or indirectly by use of a video camera. One eye can be evaluated singly by placing a gauze bandage over the opposite eye. The technique proceeds as follows. During presentation of progressively smaller targets (descending order) to the dog the target eventually becomes too small to see, and the reflex is not evoked. Likewise, during presentation of progressively larger targets (ascending order) to the dog the reflex is not evoked until a size of target is reached that can be seen by the dog. These are thresholds of visual acuity. The author's research h~s indicated that the ascending presentation probably is the superior of the two orders for visual acuity evaluation. 8 Results indicate that this technique is simple to perform, has a low variability, and is effective in discriminating abnormal function. The research also indicates that the optimum distance of the dog from the stimulus is approximately 30 em. The normal range at 30 em with ascending order of presentation is provided in Table l. 8

AUDITORY SYSTEM

The sense of hearing is the focus of a number of studies within veterinary medicine. 18 Most of these studies involve the use of the BAER, also known as the auditory brainstem response (ABR). Congenital deafness is a matter of significant concern in some breeds of dogs (e.g., Dalmatians), and acquired deafnesses caused by various conditions are relatively common. The innate behaviors that are readily adaptable to the evaluation of auditory function in veterinary medicine are the startle reflex/response and Preyer's reflex. Certainly, every veterinarian is familiar with the startle reflex. It is a memorable and often embarrassing experience to many veterinary students in their first attempt to evoke the response, trying both to remain close to the animal and out of sight as they loudly clap their hands. Preyer's reflex is less well known and is considered to be a common component of the whole complex of the startle reaction. This reflex simply

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is the pricking of the ear in response to a sound. It is observed easily in most domestic animals, particularly horses and cats. The physiology of the !itartle reflex is reviewed by several authors, whereas Preyer's reflex is less well documented. 23 The Neurologic Examination The veterinary neurologic examination includes routinely evaluating hearing using the startle reflex. As it is normally applied, it is capable of detecting the presence or absence of hearing, but it cannot determine the level of auditory acuity and usually is not used in a manner that determines the function of each ear separately. Use of the Startle Reflex and Preyer's Reflex to Evaluate Auditory Acuity The author's laboratory attempted to develop techniques to evaluate auditory acuity using the startle and Preyer's reflexes. An audiometer was used to present ascending sound stimuli at 1000 and 8000Hz. Experiments were performed in a soundproof room on both ears and each ear alone. Responses of the dogs were videotaped and evaluated by a panel. Results indicated an extremely high variability of response by individual animals between trials. Often animals failed to respond even at 11.0 dB, although all animals were shown to possess normal hearing by BAER evaluation. This failure may have been a result of the ascending order of stimulus presentation. Using the Preyer's reflex with a. randomized presentation of stimuli, others have succeeded in evaluating auditory function (frequency range) in horses. 24 The author did not use this approach because it is impractical in a clinical setting.

REFERENCES 1. Aquirre CD, Rubin LF: Progressive retinal atrophy in the miniature poodle: An electrophysiologic study. J Am Vet Med Assoc 160:191, 1972 2. Bradley RM, Mistretta CM: Intravascular taste in rats as demonstrated by conditioned aversion to sodium saccharin. J Comp Physiol Psycho! 75:186-189, 1971 3. Bromberg N, Dawson W: Preliminary measures of canine visual spatial resolution with electrophysiological techniques. In Transactions of the 11th Annual Scientific Program of the College of Veterinary Ophthalmologists, 1980 4. Cummins KA, Myers LJ: Effect of visual and olfactory alterations on social behavior of lactating dairy cows. Journal of Dairy Science 71 (suppl1):189, 1989 5. Dix MR: The mechanism and clinical significance of optokinetic nystagmus. J Laryngol Otol 94:845-864, 1980 6. Doty RL, Brugger WE, Jurs PC, et al.: Intranasal trigeminal stimulation from odorous volatiles: Psychometric responses from anosmic and normal humans. Physiol Behav 20:175-185, 1978 7. Ezeh PI, Myers LJ: Preliminary studies on the effect of steroids on olfactory function of the dog. Chemical Senses 14:698, 1989 8. Ezeh PI, Myers LJ, Cummins KA, et al: Utilizing an optokinetic device in assessing the functional visual acuity of the dog. Progress in Veterinary Neurology, in press

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9. Ferrell F: Preference for sugars and nonnutritive sweeteners in young beagles. Neurosci Biobehav Rev 8:199-203, 1984 10. Fulton AB, Hansen RM, Manning KA: Measuring visual acuity in infants. Surv Opthalmol 25:325-332, 1981 11. Ganchrow JR, Steiner JE, Daher M: Neonatal facial expressions in response to different qualities and intensities of gustatory stimuli. Infant Behavior and Development 6:189200, 1983 12. Ganong WF: Review of medical physiology, ed 13. Norwalk, CT, Appleton Lange, 1987 13. Grill HJ: The taste reactivity test: I. Mimetic responses to gustatory stimuli in neurologically normal rats. Brain Res 143:263-279, 1978 14. Hinde RA: Animal behaviour: A synthesis of ethology and comparative psychology, ed 2. New York, McGraw-Hill, 1970 15. Holloway CL: Loss of olfactory acuity in hunting animals. Auburn Vet Fall 1961:25-28, 1961 16. Johnston A, Wright MJ: Lower thresholds of motion for gratings as a function of eccentricity and contrast. Vision Res 25:179-185, 1985 17. Kay R, Palmer AC, Taylor PM: Hearing in the dog as assessed by auditory brainstem evoked potentials. Vet Rec 1984:81-84, 1984 18. Myers LJ: New techniques to evaluate sensory function in the dog. Proceedings of the Fifth Veterinary Medical Forum 5:281-284, 1987 19. Myers LJ, Boddie R, May K: Electrophysiological and innate behavioral responses of the dog to intravenous application of sweet compounds. Ann NY Acad Sci 510:519-520, 1987 20. Myers LJ, Pugh R: Thresholds of the dog for detection of inhaled eugenol and benzaldehyde determined by electroencephalographic and behavioral olfactometry. Am J Vet Res 46:2409-2412, 1985 21. Myers LJ, Hanrahan LA, Swango LJ, et al: Anosmia associated. with canine distemper. Am J Vet Res 49:1295-1297, 1988 22. Myers LJ, Nusbaum KE, Swango LJ, et al: Dysfunction of the sense of smell caused by canine parainfluenza virus infection in dogs. Am J Vet Res 49:188-190, 1988 23. Odberg FO: A study of the hearing ability of hor~es. Equine Vet J 10:82-84, 1978 24. Rashotte ME, Foster DF, Austin T: Two-pan and operant lever-press tests of dogs' preference for various foods. Neurosci Biobehav Rev 8:231-237, 1984 25. Redding RW, Braund K: The neurological examination. In Hoerlein BF (ed): Canine Neurology. Philadelphia, WB S'aunders, 1979 26. Schiffman SS: Taste and smell in disease: Part I. N Eng! J Med 308:1275-1279, 1983 27. Schwartz GJ, Grill HJ: Relationships between taste reactivity and intake in the neurologically intact rat. Chemical Senses 9:249-272, !984 28. Sireteanu R: T.he development of visual acuity in very young kittens: A study with forcedchoice preferential looking. Vision Res 25:781-788, 1985

Address reprint requests to L. J. Myers, DVM, MS, PhD 217 Greene Hall Auburn University Auburn, AL 36849-5532