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The relevance of natural stimulus patterns for sensory information processes
BRAIN RESEARCH
353
Introduction to the second session of the workshop meeting E.B.B.S. in Venice, April 23, 1971 T H E RELEVANCE OF N A T U R A L STIMULUS P A T T E R N S FOR SENSORY I N F O R M A T I O N PROCESSES
D. PLOOG Max-Planck Institute for Psychiatry, Munich (G.F.R.)
The ethological concepts of visual and auditory releasers and of the Innate Releasing Mechanism form an important part of the ethological theory of behavior. This theory is based on phylogenetic considerations, stressing the importance of evolution for species-specific behavior, or, in other words, stressing the important role of genetic factors in channeling the development of behavior. Important effects of natural selection and genetic determination on behavior are mediated through their actions on the CNS, impinging upon all levels of organization of the nervous system. Therefore, the sensory analyzer system, receiving the behavior releasing signals, should also be subject to evolution to improve their adaptive efficiency. In this context we ask ourselves what is really known about the underlying neural mechanism of the postulated Innate Releasing Mechanism, and for that matter, what relevance the natural stimulus patterns have for sensory information processes. Is there a naturalistic framework of research where the visual and auditory systems are examined while performing those functions for which they were shaped during evolution? To begin with, one might ask: What does one mean by a 'natural stimulus'? Flashes, light spots, moving lines, bars, edges, curvatures, or, tones, clicks, pips and noises are also natural since they may be seen or heard or at least may be parts of our perceptions. The term 'natural stimulus' in our context here has quite a different meaning. It is a stimulus which is linked to a certain response of the whole organism as the recipient of this stimulus. I may remind you of the famous textbook example of the herring gull chick, which directs its food begging response against the red spot on the lower tip of the yellow beak of the parent. In dummy experiments this begging response may be weakened in frequency and probably also in intensity if one or more components of this stimulus composition were omitted, and the response frequency may be increased above baseline if the feature components of the stimulus were exaggerated, e.g., if the beak is elongated and all red. This then is called a supernormal releaser for the chick's begging behavior. Because of this additive function of the parts of the stimulus composite this phenomenon is called, after Seitz, the stimulus summation effect. Brain Research, 31 (1971) 353-359
354
~ Pl~(.~
What is the neural mechanism of this behavioral response? Would it be sufficient to assume that each stimulus component triggers certain classes of neurons at the retinal and tectal level, classes of edge detectors, bar detectors, color detectors, so that the increased firing of the various populations of neurons accounts fbr the behavioral phenomenon ? If one surveys the literature on this subject, the frog and toad still seem to be among the favored animals. This is for good reason. Their sharp all-or-none movements can easily be recorded and visual stimuli can be specified in terms of retinal size, image velocity and distance since these animals remain virtually motionless prior to their prey-catching response. And their natural stimulus - - the characteristic features of a bug or worm - - is really quite simple. Nevertheless, in a carefully conducted behavioral analysis of the frog's and the toad's prey-catching, David Ingle 3 showed that the properties of this seemingly simple natural stimulus are rather complex. According to the behavior of the frog under varied experimental conditions one has to account for mechanisms of size-selectivity and also of size-constancy. Orientation was readily elicited by white shadowless moving edges, which is not in accordance with the weak retinal unit responses to such stimuli. Also contrary to the behavior of certain unit classes is the observation that both frogs and toads respond better to an object with a withdrawing edge than to an advancing one. On the other hand, the preference for withdrawing edges does not hold when two moving edges are present. For example, toads orient chiefly to the head of a worm. The interaction of two edges of a moving stimulus is not predictable from knowledge of the frog's response to objects with a single moving edge. Ingle states explicitly 3 that visual identification of objects often involves 'non-additivity of the parts', and recalls the many examples of Gestalt psychology. From Ingle's data one must admit only partial correspondence between the stimulus optimal for retinal ganglion units and the preferences of the whole frog. This may not be surprising if one assumes with the Grfissers that the fi'og retina is only a first-stage filter of sensory information within a multilayered system. A detailed analysis of the optic tectum leads a step further. I have selected this example for two reasons. First, the best response of a neuron to a certain stimulus, such as a convex edge, does not necessarily mean that this stimulus characteristic is essential for the explanation of the frog's visual selectivity. It merely means that this stimulus configuration fires certain classes of units under certain conditions during information processing. Lettvin and Maturana have called this the filtering of 'useful parcels of information.' Second, and perhaps more related to the relevance of a natural stimulus, the detailed analysis of a behavioral response is essential for the proper description of the features of a natural stimulus. For example, in dummy experiments like Ingle's the stimulus features of the dummy must be adequate for the elicitation of the behavior under investigation. Then, and only then, meaningful correlations between behavioral and neurophysiological data can be made. Admittedly, this is a strong statement which I hope will be challenged by the electrophysiologists. I do not want to speak of non-sensory conditions for the relevance of natural Brain Research, 31 (1971) 353-359
SENSORY 1NFORMA]ION PROCESSES
355
stimuli and will mention only in passing that the frog does not jump at the bug in his visual field when he has a full stomach. What does the visual system do under this condition? I also cannot go into the problems dealing with the relevance of natural stimuli for mammals, especially for the young monkey and the human baby where rapid learning is such an important parameter. I may just say that Sackett's findings on his so-called 'picture-input-isolated' rhesus monkey infants have shown that the threatening face of an adult monkey's picture - - and not other monkey pictures - causes fearful behavior in the isolated baby after its third month of life. Sackett interprets this finding as the maturation of an innate releasing mechanism for facial expressions. For dummy experiments in the human baby it is also known that the response pattern to facial expressions changes during early develoFment. There was a longlasting dispute between learning psychologists and ethologists as to whether smiling is a social releaser or a learned response. If it were altogether learned, it would be very difficult to explain the full smile of a blind baby of 4 weeks of age. The point here is that the presence c f a social signal, such as the smile, indicates also the presence of an analyzer system that processes the information transmitted by the social signal. However, since nothing is known about the underlying neural mechanisms for the information processing of the facial expression in primates, it is very difficult indeed to speculate about this. Let us now discuss the auditory system. In terms of evolutionary development, hearing is the most recent of the special senses, and holds a special interest because of its relationship to that most unique characteristic of the human being, his capacity for language 7. The organization of the auditory system is quite different from the visual one. At the input level, there are in one human retina about 130 million rods and cones which feed into a million optic nerve fibers. In one human cochlea there are 30 thousand hair cells which feed into 30 thousand fibers in the cochlear nerve. The ratio of receptors to nerve fibers is therefore 130 : I for vision, but only I : 1 for audition*. The larger number of receptor units for vision clearly reflects the fact that the point-topoint detection of a spatial display requires more simultaneous receptor action, whereas for acoustic stimuli, less information is presented simultaneously, and the pattern over time can be analyzed by fewer receptors responding to serial changes. The ratio of optic nerve fibers to subcortical ceils is between 2 : 1 and 1 : 1. In contrast 30 thousand fibers of the auditory nerve feed into about I million subcortical neurons on one side of the auditory pathway. Thus, the ratio of nerve fibers to subcortical cells is I : 33 for audition. And finally, the ratio of nerve fibers to cortical cells are, respectively, 1 : 540 for vision, and 1 : 3,300 for audition. Supplementing this disparity is the fact that auditory cortex has twice as many synapses per unit volume as visual cortex (Worden). It would be tempting to compare the striking structural differences * However, it should be pointed out that the analogue of the cochlear nerve is presumably the coupling layers within the retina.
Brain Research, 3l (1971) 353 359
356
~ H.(~(~(~
of the two systems - - mainly on the input levet and in the cortex ~ ~<~re closely ( ~ functional considerations. I have mentioned these few tigures in order to gt~ard agaillst the general idea that principles of visual information processing are rcad il? applicable to the information processing of auditory signals. However, when it comes to the relevance of natural stimulus patterns, c o ~ parisons between the two systems are certainly possible. Let us again take the frog as an illustration. For the adult bullfrog there are two frequency peaks in the mating call, one at about 200 c/sec and one at about 1,500 c/sec with a deep dip at 500 c/sec. These two peaks together constitute the optimum stimulus for evoking an approach response in the female frog. in the >'~mng malc frogs, the frequency of the lower peak is higher than in the adult, t h ~ is, close Io 500 c/sec. As the frog matures, this lower peak frequency gradually drops until it reaches 200 c/sec. In parallel with this maturational shift of the lower [~eak fi'equency, there is a corresponding increase in the capacity of the young frog's caii to attract females. Corresponding to the work of Capranica. Gerstein and Frishkopf recorded from the frog's hearing organ. They identified so-called simple units with the basilar papilla and so-called complex units with the amphibian papilla. The lalter receptor elements respond at 200 c/sec whereas the basilar papilla responds at 1,500 c/see. Thus, the receptor organ of the frog presents a two-peaked spectrum of acoustic energy to its nervous system. The peaks in this filter system correspond with the peaks of energy in the spectrogram of the bullfrog croak. The dip in the spectrogram at 500 c/see is significant in that acoustic energies at this frequency cause inhibition ~H co~nplex receptive units. This means for the natural situation that the croak of the immature male frog falls in the dip zone which inhibits the response of complex receptive units in the female which suggest that this may be one mediating ~r~echanism c~ntributing to the failure ofgravid females to respond to the calls e f i m m a t u r e males. A 5(;0 c/~e~ tone also stops the adult males' calling. Consequently, there might possibly be a neural unit upon which the low f r c quency and the high frequency peaks must converge to evoke a response fi'om the female. A search for this 'croak detector' neuron was conducted by Frishkopt'. He found units in the subtectal region which would respond either to low or to high frequency, but no unit was found anywhere whose response depended upon a convergence of both peak frequencies. The question of whether it is plausible to look for such a unit leads into the entire conceptual problem concerning the role of the so-called featuredetector neurons (rather trigger features) in hearing which I will not deal with since it will certainly come up again in the discussion periods during the meeting. The frog croak example was chosen because of its simplicity. It demonstrates the chief features of a natural stimulus pattern. It also shows the species-specific. that is, genetically determined, biological significance of the stimulus, and its brings out a striking correspondence between the physical characteristics of the natural stimulus and the neural organization at receptor level, which, in ethological terms, might be thought of as the first stage of an innate releasing mechanism, the proper croak being the releasing stimulus. It is not only of historical interest but also of conBrain Research, 31 (1971) 353-359
SENSORY INFORMATION PROCESSES
357
ceptual importance that Lorenz and later also Tinbergen and others have explicitly spoken of an innate releasing mechanism as a possible filter mechanism long before an adequate neurophysiology for testing such a hypothesis was available. Another term must be discussed because of its relation to the innate releasing mechanism and its conceptual implications. It is the term 'template' which is mostly used with reference to song birds. But 1 believe that the concept behind this term is also relevant for mammalian and in particular for primate auditory behavior. Template refers to internal mechanisms which enable particular elements within the total auditory input to selectively evoke behavioral response because they match the template features. The template may be genetically predetermined or may require auditory experience for its development. From studies in birds 3 types of template formation may be distinguished : (1) Some birds (e.g., domestic fowl) will produce the species-specific call even if deafened at birth prior to exposure to the call. This implies a pre-wired, genetically determined motor model for a call production. There is no process of matching to an auditory input. (2) Some birds (e.g., song sparrows) can develop the normal song even though raised in isolation from it, but, if deafened at birth, the normal song fails to develop, suggesting that auditory feedback from their own song production is necessary, presumably for matching with a template. (3) In the third type of ontogeny, not only is auditory feedback necessary, but also an external 'model' of the correct song must be presented to the developing bird. For example, chaffinches raised in isolation have abnormal songs which lack much of the structure which forms when they are exposed to the species-specific song during development. In the second case of the song sparrow the natural stimulus pattern, i.e., the species-specific song not only transmits information to the con-specifics but also serves as the adequate stimulus for their own production of that pattern. In the third case with the chaffinch as an example not only is feedback from their own song necessary for the correct development of the natural stimulus but also tradition is needed, i.e., for the correct call to develop parents must give an example for the offspring. As before when I discussed the visual releasers, I must make a jump across the phylogenetical scale to say a few words about monkeys. To my knowledge no one really knows whether a monkey deafened at birth will produce his species-specific calls. The sparse experience with deafening of squirrel monkeys which we have gained in our laboratory has shown that there is no appreciable deterioration in the quality of the many calls that this species inherits. However, the deafened animals were adults. The age of deafening may not only be important for certain birds and man but also for the monkey. Furthermore, we know from the squirrel monkey that he emits calls, such as certain peeps, right after birth, and a noticeable proportion of his vocal repertoire can be heard - - and is responded to by mother and cagemates - - within the first week'of life. We also know that all the approximately 30 different calls are rather stereotyped and easy to identify from sound spectrograms, and we know that
Brain Research, 31 (197l) 353-359
358
~ Pt (~>(
all of them can be electrically evoked from definable brain sites. Man3 ot ~he calls a~'c rather well known with respect to their signal function. In terms of the template concept there is evidence that this srecies iits best the first type, that is a genetically determined motor model for the call production. There is probably no process of matching to an auditory input. Whether this is true for other non-human primates remains to be investigated. In the case of humans the situation is obviously fundamenlall3 different. Without even beginning to discuss any aspects of language and speech one would be inclined to discard a concept that resembles a template. But is this really so'? If ranguage has a biological foundation and if there are the universals of language in the Chomsky sense of the word then it is likely that these features, common 1o all languages, should be reflected at a very basic, one might say neurological, ievel. This appears to be the case at the level of the generation and rerception (~f phonemes. Liberman and his colleagues at the Haskin Laboratories in New Haven, Conn. have shown that there is no simple I : I relationship between patterns of acoustic energy and perception of the speech sound. For example, the acoustic pattern underlying the phonemes 'di' and 'du' are different in the second formant whereby the FM transition of the 'd' in 'di' is upward and in 'd' in 'dtl' it is downward across frequenc3. These same FM transitions if presented in a non-speech context, are heard respectively as an ascending or descending chirp or trill, neither of which is perceived in the speech context where the percept is always 'd'. It also has been demonstrated that the perception of speech sounds is categorical in that graded variation in the acoustic patterns do not give rise to graded percepts in the linguistic mode. To put it another way, the discrimination of speech sounds occurs not within phonemic boundaries but between phonemic boundaries. On these grounds rather sophisticated experiments of speech perception in 1-4 month-old infants have been conducted recently. The speech sounds ~aried along an acoustic dimension previously shown to cue phonemic distinctions in adults. Discrimination was measured by a special conditioning technique with sucking as the response. The outcome is rather impressive. The results strongly indicate that infants as young as one month of age are not only responsive to speech sounds and able to make fine discriminations but are also perceiving speech sounds along the voicing continuum in the same manner in which adults perceive these sounds. Another way of stating this effect is that infants are able to sort acoustic variations of adult phonemes into categories. Peter Eimas and co-workers conclude that the means by which the perception in a linguistic mode is accomplished may well be part of the biological makeup of the organism and that these means must be operative at an unexpectedly early age. To relate this result to the relevance of natural stimulus patterns for sensory information processes we may just repeat what has been said about I the template. It refers to whatever internal mechanism enables particular elements within the total auditory input to selectively evoke behavioral response because they match the template features. In closing, 1 want to paraphrase what I intended to convey by quoting Donald Brain Research, 31 (1971) 353-359
SENSORY INFORMATION PROCESSES
359
MacKay who said in 1956, 'One has to drop the idea that perception is the witnessing of incoming signals, and instead think of perception as an internal adaptive reaction to the demands made by the world by way of the receptive organs'.
REFERENCES 1 EIMAS, P. D., SIGUELANO, E. R., JUSCZYK, P., AND VIGORITO, J., Speech perception in infants, Science, 171 (1971) 303-306. 2 GALAMBOS, R., AND WORDEN, F. G., Auditory processing of biologically significant sounds, Neurosci. Res. Progr. Bull., (1971) in preparation. 3 INGLE, D., Visual releasers of prey-catching behavior in frogs and toads, Brain, Behav., Evol., 1 (1968) 500- 518, 4 MACKAY, D. M., A mind's eye view of the brain. In N. WIENER AND J. P. SCI-IADI~(Eds.), Cybernetics of the Nervous System, Progress in Brain Research, Vol. 17, (1965) 321-332. 5 PLOOG, D., AND MELNECHUK, T., Primate communication, Neurosci. Res. Progr., 7 (1969) 419-510, 6 PLOOG, D., Social communication among animals. In F. O. SCHMITT (Ed.), The Neuroscienees: Second Study Program, Rockefeller Univ. Press, New York, 1970. 7 WORDEN,F. G., Hearing and the neural detection of acoustic patterns, Behav. Sci., 16 (1971) 20-30.
Brain Research, 31 (1971) 353- 359
353
Introduction to the second session of the workshop meeting E.B.B.S. in Venice, April 23, 1971 T H E RELEVANCE OF N A T U R A L STIMULUS P A T T E R N S FOR SENSORY I N F O R M A T I O N PROCESSES
D. PLOOG Max-Planck Institute for Psychiatry, Munich (G.F.R.)
The ethological concepts of visual and auditory releasers and of the Innate Releasing Mechanism form an important part of the ethological theory of behavior. This theory is based on phylogenetic considerations, stressing the importance of evolution for species-specific behavior, or, in other words, stressing the important role of genetic factors in channeling the development of behavior. Important effects of natural selection and genetic determination on behavior are mediated through their actions on the CNS, impinging upon all levels of organization of the nervous system. Therefore, the sensory analyzer system, receiving the behavior releasing signals, should also be subject to evolution to improve their adaptive efficiency. In this context we ask ourselves what is really known about the underlying neural mechanism of the postulated Innate Releasing Mechanism, and for that matter, what relevance the natural stimulus patterns have for sensory information processes. Is there a naturalistic framework of research where the visual and auditory systems are examined while performing those functions for which they were shaped during evolution? To begin with, one might ask: What does one mean by a 'natural stimulus'? Flashes, light spots, moving lines, bars, edges, curvatures, or, tones, clicks, pips and noises are also natural since they may be seen or heard or at least may be parts of our perceptions. The term 'natural stimulus' in our context here has quite a different meaning. It is a stimulus which is linked to a certain response of the whole organism as the recipient of this stimulus. I may remind you of the famous textbook example of the herring gull chick, which directs its food begging response against the red spot on the lower tip of the yellow beak of the parent. In dummy experiments this begging response may be weakened in frequency and probably also in intensity if one or more components of this stimulus composition were omitted, and the response frequency may be increased above baseline if the feature components of the stimulus were exaggerated, e.g., if the beak is elongated and all red. This then is called a supernormal releaser for the chick's begging behavior. Because of this additive function of the parts of the stimulus composite this phenomenon is called, after Seitz, the stimulus summation effect. Brain Research, 31 (1971) 353-359
354
~ Pl~(.~
What is the neural mechanism of this behavioral response? Would it be sufficient to assume that each stimulus component triggers certain classes of neurons at the retinal and tectal level, classes of edge detectors, bar detectors, color detectors, so that the increased firing of the various populations of neurons accounts fbr the behavioral phenomenon ? If one surveys the literature on this subject, the frog and toad still seem to be among the favored animals. This is for good reason. Their sharp all-or-none movements can easily be recorded and visual stimuli can be specified in terms of retinal size, image velocity and distance since these animals remain virtually motionless prior to their prey-catching response. And their natural stimulus - - the characteristic features of a bug or worm - - is really quite simple. Nevertheless, in a carefully conducted behavioral analysis of the frog's and the toad's prey-catching, David Ingle 3 showed that the properties of this seemingly simple natural stimulus are rather complex. According to the behavior of the frog under varied experimental conditions one has to account for mechanisms of size-selectivity and also of size-constancy. Orientation was readily elicited by white shadowless moving edges, which is not in accordance with the weak retinal unit responses to such stimuli. Also contrary to the behavior of certain unit classes is the observation that both frogs and toads respond better to an object with a withdrawing edge than to an advancing one. On the other hand, the preference for withdrawing edges does not hold when two moving edges are present. For example, toads orient chiefly to the head of a worm. The interaction of two edges of a moving stimulus is not predictable from knowledge of the frog's response to objects with a single moving edge. Ingle states explicitly 3 that visual identification of objects often involves 'non-additivity of the parts', and recalls the many examples of Gestalt psychology. From Ingle's data one must admit only partial correspondence between the stimulus optimal for retinal ganglion units and the preferences of the whole frog. This may not be surprising if one assumes with the Grfissers that the fi'og retina is only a first-stage filter of sensory information within a multilayered system. A detailed analysis of the optic tectum leads a step further. I have selected this example for two reasons. First, the best response of a neuron to a certain stimulus, such as a convex edge, does not necessarily mean that this stimulus characteristic is essential for the explanation of the frog's visual selectivity. It merely means that this stimulus configuration fires certain classes of units under certain conditions during information processing. Lettvin and Maturana have called this the filtering of 'useful parcels of information.' Second, and perhaps more related to the relevance of a natural stimulus, the detailed analysis of a behavioral response is essential for the proper description of the features of a natural stimulus. For example, in dummy experiments like Ingle's the stimulus features of the dummy must be adequate for the elicitation of the behavior under investigation. Then, and only then, meaningful correlations between behavioral and neurophysiological data can be made. Admittedly, this is a strong statement which I hope will be challenged by the electrophysiologists. I do not want to speak of non-sensory conditions for the relevance of natural Brain Research, 31 (1971) 353-359
SENSORY 1NFORMA]ION PROCESSES
355
stimuli and will mention only in passing that the frog does not jump at the bug in his visual field when he has a full stomach. What does the visual system do under this condition? I also cannot go into the problems dealing with the relevance of natural stimuli for mammals, especially for the young monkey and the human baby where rapid learning is such an important parameter. I may just say that Sackett's findings on his so-called 'picture-input-isolated' rhesus monkey infants have shown that the threatening face of an adult monkey's picture - - and not other monkey pictures - causes fearful behavior in the isolated baby after its third month of life. Sackett interprets this finding as the maturation of an innate releasing mechanism for facial expressions. For dummy experiments in the human baby it is also known that the response pattern to facial expressions changes during early develoFment. There was a longlasting dispute between learning psychologists and ethologists as to whether smiling is a social releaser or a learned response. If it were altogether learned, it would be very difficult to explain the full smile of a blind baby of 4 weeks of age. The point here is that the presence c f a social signal, such as the smile, indicates also the presence of an analyzer system that processes the information transmitted by the social signal. However, since nothing is known about the underlying neural mechanisms for the information processing of the facial expression in primates, it is very difficult indeed to speculate about this. Let us now discuss the auditory system. In terms of evolutionary development, hearing is the most recent of the special senses, and holds a special interest because of its relationship to that most unique characteristic of the human being, his capacity for language 7. The organization of the auditory system is quite different from the visual one. At the input level, there are in one human retina about 130 million rods and cones which feed into a million optic nerve fibers. In one human cochlea there are 30 thousand hair cells which feed into 30 thousand fibers in the cochlear nerve. The ratio of receptors to nerve fibers is therefore 130 : I for vision, but only I : 1 for audition*. The larger number of receptor units for vision clearly reflects the fact that the point-topoint detection of a spatial display requires more simultaneous receptor action, whereas for acoustic stimuli, less information is presented simultaneously, and the pattern over time can be analyzed by fewer receptors responding to serial changes. The ratio of optic nerve fibers to subcortical ceils is between 2 : 1 and 1 : 1. In contrast 30 thousand fibers of the auditory nerve feed into about I million subcortical neurons on one side of the auditory pathway. Thus, the ratio of nerve fibers to subcortical cells is I : 33 for audition. And finally, the ratio of nerve fibers to cortical cells are, respectively, 1 : 540 for vision, and 1 : 3,300 for audition. Supplementing this disparity is the fact that auditory cortex has twice as many synapses per unit volume as visual cortex (Worden). It would be tempting to compare the striking structural differences * However, it should be pointed out that the analogue of the cochlear nerve is presumably the coupling layers within the retina.
Brain Research, 3l (1971) 353 359
356
~ H.(~(~(~
of the two systems - - mainly on the input levet and in the cortex ~ ~<~re closely ( ~ functional considerations. I have mentioned these few tigures in order to gt~ard agaillst the general idea that principles of visual information processing are rcad il? applicable to the information processing of auditory signals. However, when it comes to the relevance of natural stimulus patterns, c o ~ parisons between the two systems are certainly possible. Let us again take the frog as an illustration. For the adult bullfrog there are two frequency peaks in the mating call, one at about 200 c/sec and one at about 1,500 c/sec with a deep dip at 500 c/sec. These two peaks together constitute the optimum stimulus for evoking an approach response in the female frog. in the >'~mng malc frogs, the frequency of the lower peak is higher than in the adult, t h ~ is, close Io 500 c/sec. As the frog matures, this lower peak frequency gradually drops until it reaches 200 c/sec. In parallel with this maturational shift of the lower [~eak fi'equency, there is a corresponding increase in the capacity of the young frog's caii to attract females. Corresponding to the work of Capranica. Gerstein and Frishkopf recorded from the frog's hearing organ. They identified so-called simple units with the basilar papilla and so-called complex units with the amphibian papilla. The lalter receptor elements respond at 200 c/sec whereas the basilar papilla responds at 1,500 c/see. Thus, the receptor organ of the frog presents a two-peaked spectrum of acoustic energy to its nervous system. The peaks in this filter system correspond with the peaks of energy in the spectrogram of the bullfrog croak. The dip in the spectrogram at 500 c/see is significant in that acoustic energies at this frequency cause inhibition ~H co~nplex receptive units. This means for the natural situation that the croak of the immature male frog falls in the dip zone which inhibits the response of complex receptive units in the female which suggest that this may be one mediating ~r~echanism c~ntributing to the failure ofgravid females to respond to the calls e f i m m a t u r e males. A 5(;0 c/~e~ tone also stops the adult males' calling. Consequently, there might possibly be a neural unit upon which the low f r c quency and the high frequency peaks must converge to evoke a response fi'om the female. A search for this 'croak detector' neuron was conducted by Frishkopt'. He found units in the subtectal region which would respond either to low or to high frequency, but no unit was found anywhere whose response depended upon a convergence of both peak frequencies. The question of whether it is plausible to look for such a unit leads into the entire conceptual problem concerning the role of the so-called featuredetector neurons (rather trigger features) in hearing which I will not deal with since it will certainly come up again in the discussion periods during the meeting. The frog croak example was chosen because of its simplicity. It demonstrates the chief features of a natural stimulus pattern. It also shows the species-specific. that is, genetically determined, biological significance of the stimulus, and its brings out a striking correspondence between the physical characteristics of the natural stimulus and the neural organization at receptor level, which, in ethological terms, might be thought of as the first stage of an innate releasing mechanism, the proper croak being the releasing stimulus. It is not only of historical interest but also of conBrain Research, 31 (1971) 353-359
SENSORY INFORMATION PROCESSES
357
ceptual importance that Lorenz and later also Tinbergen and others have explicitly spoken of an innate releasing mechanism as a possible filter mechanism long before an adequate neurophysiology for testing such a hypothesis was available. Another term must be discussed because of its relation to the innate releasing mechanism and its conceptual implications. It is the term 'template' which is mostly used with reference to song birds. But 1 believe that the concept behind this term is also relevant for mammalian and in particular for primate auditory behavior. Template refers to internal mechanisms which enable particular elements within the total auditory input to selectively evoke behavioral response because they match the template features. The template may be genetically predetermined or may require auditory experience for its development. From studies in birds 3 types of template formation may be distinguished : (1) Some birds (e.g., domestic fowl) will produce the species-specific call even if deafened at birth prior to exposure to the call. This implies a pre-wired, genetically determined motor model for a call production. There is no process of matching to an auditory input. (2) Some birds (e.g., song sparrows) can develop the normal song even though raised in isolation from it, but, if deafened at birth, the normal song fails to develop, suggesting that auditory feedback from their own song production is necessary, presumably for matching with a template. (3) In the third type of ontogeny, not only is auditory feedback necessary, but also an external 'model' of the correct song must be presented to the developing bird. For example, chaffinches raised in isolation have abnormal songs which lack much of the structure which forms when they are exposed to the species-specific song during development. In the second case of the song sparrow the natural stimulus pattern, i.e., the species-specific song not only transmits information to the con-specifics but also serves as the adequate stimulus for their own production of that pattern. In the third case with the chaffinch as an example not only is feedback from their own song necessary for the correct development of the natural stimulus but also tradition is needed, i.e., for the correct call to develop parents must give an example for the offspring. As before when I discussed the visual releasers, I must make a jump across the phylogenetical scale to say a few words about monkeys. To my knowledge no one really knows whether a monkey deafened at birth will produce his species-specific calls. The sparse experience with deafening of squirrel monkeys which we have gained in our laboratory has shown that there is no appreciable deterioration in the quality of the many calls that this species inherits. However, the deafened animals were adults. The age of deafening may not only be important for certain birds and man but also for the monkey. Furthermore, we know from the squirrel monkey that he emits calls, such as certain peeps, right after birth, and a noticeable proportion of his vocal repertoire can be heard - - and is responded to by mother and cagemates - - within the first week'of life. We also know that all the approximately 30 different calls are rather stereotyped and easy to identify from sound spectrograms, and we know that
Brain Research, 31 (197l) 353-359
358
~ Pt (~>(
all of them can be electrically evoked from definable brain sites. Man3 ot ~he calls a~'c rather well known with respect to their signal function. In terms of the template concept there is evidence that this srecies iits best the first type, that is a genetically determined motor model for the call production. There is probably no process of matching to an auditory input. Whether this is true for other non-human primates remains to be investigated. In the case of humans the situation is obviously fundamenlall3 different. Without even beginning to discuss any aspects of language and speech one would be inclined to discard a concept that resembles a template. But is this really so'? If ranguage has a biological foundation and if there are the universals of language in the Chomsky sense of the word then it is likely that these features, common 1o all languages, should be reflected at a very basic, one might say neurological, ievel. This appears to be the case at the level of the generation and rerception (~f phonemes. Liberman and his colleagues at the Haskin Laboratories in New Haven, Conn. have shown that there is no simple I : I relationship between patterns of acoustic energy and perception of the speech sound. For example, the acoustic pattern underlying the phonemes 'di' and 'du' are different in the second formant whereby the FM transition of the 'd' in 'di' is upward and in 'd' in 'dtl' it is downward across frequenc3. These same FM transitions if presented in a non-speech context, are heard respectively as an ascending or descending chirp or trill, neither of which is perceived in the speech context where the percept is always 'd'. It also has been demonstrated that the perception of speech sounds is categorical in that graded variation in the acoustic patterns do not give rise to graded percepts in the linguistic mode. To put it another way, the discrimination of speech sounds occurs not within phonemic boundaries but between phonemic boundaries. On these grounds rather sophisticated experiments of speech perception in 1-4 month-old infants have been conducted recently. The speech sounds ~aried along an acoustic dimension previously shown to cue phonemic distinctions in adults. Discrimination was measured by a special conditioning technique with sucking as the response. The outcome is rather impressive. The results strongly indicate that infants as young as one month of age are not only responsive to speech sounds and able to make fine discriminations but are also perceiving speech sounds along the voicing continuum in the same manner in which adults perceive these sounds. Another way of stating this effect is that infants are able to sort acoustic variations of adult phonemes into categories. Peter Eimas and co-workers conclude that the means by which the perception in a linguistic mode is accomplished may well be part of the biological makeup of the organism and that these means must be operative at an unexpectedly early age. To relate this result to the relevance of natural stimulus patterns for sensory information processes we may just repeat what has been said about I the template. It refers to whatever internal mechanism enables particular elements within the total auditory input to selectively evoke behavioral response because they match the template features. In closing, 1 want to paraphrase what I intended to convey by quoting Donald Brain Research, 31 (1971) 353-359
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MacKay who said in 1956, 'One has to drop the idea that perception is the witnessing of incoming signals, and instead think of perception as an internal adaptive reaction to the demands made by the world by way of the receptive organs'.
REFERENCES 1 EIMAS, P. D., SIGUELANO, E. R., JUSCZYK, P., AND VIGORITO, J., Speech perception in infants, Science, 171 (1971) 303-306. 2 GALAMBOS, R., AND WORDEN, F. G., Auditory processing of biologically significant sounds, Neurosci. Res. Progr. Bull., (1971) in preparation. 3 INGLE, D., Visual releasers of prey-catching behavior in frogs and toads, Brain, Behav., Evol., 1 (1968) 500- 518, 4 MACKAY, D. M., A mind's eye view of the brain. In N. WIENER AND J. P. SCI-IADI~(Eds.), Cybernetics of the Nervous System, Progress in Brain Research, Vol. 17, (1965) 321-332. 5 PLOOG, D., AND MELNECHUK, T., Primate communication, Neurosci. Res. Progr., 7 (1969) 419-510, 6 PLOOG, D., Social communication among animals. In F. O. SCHMITT (Ed.), The Neuroscienees: Second Study Program, Rockefeller Univ. Press, New York, 1970. 7 WORDEN,F. G., Hearing and the neural detection of acoustic patterns, Behav. Sci., 16 (1971) 20-30.
Brain Research, 31 (1971) 353- 359