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Evoked responses in the chicken telencephalon to auditory, visual, and tactile stimulation
EXPERIMENTAL
Evoked
KEUROLOGY
17,
495-504
Responses Auditory, NORMA
in the Visual,
Chicken
and
Tactile
Telencephalon
to
Stimulation
ADAMO AND ROBERT L. KING’
JEAN
Departments of Anatomy U&ersity of Florida
(1967)
and
Physiology and Center for Neurobiological Sciences, College of Medicine, Gainesville, Florida 32603
Received
December
22. 1966
Auditory, visual and cutaneous electrical stimulations were administered to anesthetized chickens and the evoked responses to each stimulus modality was systematically recorded from the cerebral hemispheres. Principal responses to auditory stimulation were observed predominantly from the Wulst (dorsomedial sagittal elevation of the avian forebrain). Application of 1% procaine to the surface of the Wulst either decreased or abolished the response, indicating that the Wulst has a functional anatomical role in the chicken’s auditory system. Responses to photic stimulation also were recorded from the Wulst and surrounding hemispheric areas. Since topical application of 1% procaine to the cerebral hemispheres did not alter the visually evoked responses, forebrain structures responsible for these responses are thought to be in areas other than the Wulst. Cutaneous electrical stimulation was not found to produce responses from the Wulst or surrounding hemispheric areas. The characteristics of the responses obtained in birds to auditory stimulation are compared to those reported for the alligalor. The differences found suggest that the avian Wulst functions differently from the reptilian “general cortex” with respect to the auditory system. The present observations in birds are interpreted to indicate that the Wulst is related to the auditory system by fiber connections which have relatively few synapses. Introduction
Direct anatomical evidence for termination of the auditory, visual and tactile systems in the avian forebrain has yet to be unequivocally established. From an extensive electrophysiological study of auditory and tactile relays in the pigeon, Erulkar (1) was able to determine that certain regions of the brain stem and cerebral hemispheres were activated by tactile and auditory stimulation. Both stimulus modalities were found to evoke responses from discrete areas in the neostriatum caudale, but not from the hyperstriatum. 1 This work was supported Blindness, National Institutes of received support from Training Henry R. Wilson for his help Dept. of Anatomy, University Mexico 87106.
by the National Institute of Neurological Diseases and Health, under Grants NB-3990 and NB-1548. Dr. Adamo Grant Z-TIGM-579. The authors are indebted to Dr. in supplying animals. Dr. Adamo’s present address is: of New Mexico School of Medicine, Albuquerque, New
498
CHICKEN
TELENCEPH.ALON
499
Rougeul (S), also working with pigeons, presented evidence that visual stimulation activates areas of the forebrain immediately below the \Yulst (dorsomedial sagittal elevation of the avian forebrain). Gogan (2) found polysensory units in the pigeon telencephalon which were responsive to light, sound and somesthetic stimulation; the location of these polysensory units were not indicated. The present study was undertaken to determine if the Wulst may participate as a functional anatomical component in the auditory. visual and tactile systems in the chicken. Materials
and
Methods
Thirty-nine adult chickens between the ages of 12 and 20 weeks were used in this study. Chloralose anesthesia (100 mg kg) was administered intramuscularly and gallamine triethiodide (3-5 mg,, kg, im or iv) was given as needed for immobilization. The birds were maintained on artificial respiration and their heads fixed in position. The hemispheres were exposed and the Wulst and surrounding hemispheric areas explored monopolarly with KClfilled capillary microelectrodes with 3-5 p diameter tips. Amplification was through an a-c coupled amplifier system with cathode follower. .L\ll responses were observed on a dual beam cathode ray oscilloscope and many cases were averaged by a (CAT) computer before permanent recordings were made photographically. Auditory stimuli were produced by feedin g O.l-msec square waves into a speaker. The resulting clicks were delivered at 4-set intervals to the left ear through a plastic tube leading from the speaker to the bird’s ear. Xo attempt was made to seal off or deafen the right ear; therefore it is assumed that stimulation was to some extent bilateral. Single Aash photic stimuli were given simultaneously to both eyes with a pulsed strobe light at a distance of approximately 45.5 cm. Single shock cutaneous stimuli (approsimately lol.Sv, 1-msec duration) were delivered through closely spaced needle electrodes placed at numerous positions on the body surface. Results
The Wulst is a three-layered elevated area on the dorsomedial surface of the avian neopallium. It contains the accessory hyperstriatum (immediately subjacent to the superficial corticoid layer), the dorsal hyperstriatum (deepest of the three layers), and the nucleus intercalatus (situated between the accessory and dorsal hyperstriata). Immediately below the Wulst is the ventral hyperstriatum (Fig. 1). Externally, the \Vulst is separated from the remainder of the hemisphere by a fissure, the vallecula. The majority of the electrode points explored in and around the U’ulst were tested with auditory (click), photic, and cutaneous electrical stimulation. Responses evoked by click stimulation were primarily surface positive.
500
ADAM0
AND
KING
FIG. 1. Sagittal section through the chicken hyperstriatum; X.1., nucleus intercalatus; D.H., hyperstriatum; S, neostriatum; P, paleostriatum; Wulst consists of the accessory hyperstriatum, the intercalatus.
brain. -4bbreviations: .4.H.. accessor dorsal hyperstriatum; V.H.. ventral .4, archistriatum; V, ventricle. The dorsal hyperstriatum, and the nucleus
consisting of either a single positive component followed by a small negative slow wave, or of a group of two to three brief positive-negative components, again followed by a small negative slow wave. Most of the responsesobserved were of the former type (Fig. 2, left). Latencies of the majority of the responsesrecorded from the Wulst were in the range of 5-8 msec though a few responses,mainly from caudal areas,had latenciesaslong as 14 msec.Duration of the auditory responseswas usually about 20 msec. At the caudal boundary of the Wulst, an occasional responsewas recorded which showed a much more pronounced surface negativity. These responseswere longer in latency (14-20 msec) with a negative component lasting for approximately 40 msec. The few responsesto click stimulation obtained outside the Wulst were of smaller amplitude than those found within the Wulst, and were much less reliably present. Responsesof this kind were found in the only hemispheric area immediately caudal to the Wulst. Responsesto photic stimulation were found throughout the hemispheres. Such responseswere of longer latency (IO-20 msec), longer duration (up to 150 msec), and larger amplitude than the responsesobtained with auditory stimulation. Photic responsestypically exhibited an initial surface negativity, followed by a longer lasting positive-negative complex (Fig. 2, right ). Activation of the telencephalon by cutaneous electrical stimulation was found in only one electrode tract, and that only at a depth of 3200 p (below the Wulst proper, and probably in the neostriatum). The remainder
CHICKEN
TELENCEPHALON
F1c:. _. 3 Left column: Evoked responses t\veen pulses, .5 msec; calibration, 100 kv. Cup~wr) and acoustic (middle1 stimulation;
in \Vulst to acoustic stimulation; Right column: Evoked rcsponscs calibration, 100 !LV.
SO1
time beto photic
of the hemispheric surface and its underlying structures were found to show responses only to auditory and photic stimulation. Responses exhibiting initially surface-positive activity to auditory stimulation and initially surface-negative activity to photic stimulation were recorded from identical points in the area of the R’ulst. Depth recording typically showed a decrease in amplitude of the auditory responses at 200-300 11sometimes, though rarely, associated with a reversal to initial negativity. Below this level the initial positivity returned, with a decrease in the succeeding negative wave until a point (about 2 800 10 was reached below the level of the L\‘ulst proper (Fig. 3)! Application to the surface of the LVulst of small bits of filter paper soaked in lc/r procaine solution decreased or abolished the surface response to auditory stimulation, indicating that the superficial layers are active in auditory function. Following application of 17; procaine responses to photic stimulation were not affected in any way, suggesting that these responses have their origin somewhere in deeper structures of the forebrain.
502
ADAM0
AND
depths
through
KING
SURF
200 400
800
1200 1.600
2000
2400
2800 3200
3600
4000
FIG.
CAT
3. Responses at varyinp computer for one trace).
the
Wulst
(25
responses
averaged
by
CHICKEN
TELENCEPH.ALOS
503
Discussion
As far rostrally as the auditory pathways have been histologically determined, the available morphological data indicate that the afferent systems of birds and reptiles are almost identical. However. electro-anatomical studies by Moore and Tschirgi (4) show that in the reptile (alligator) telencephalon. visual, auditory and tactile stimulation will elicit responses bilaterally and diffusely throughout the “general cortex” described by Kappers, Huber and Crosby (3). These polysensory responses have long latencies (SO-100 msec) and become rapidly attenuated or habituated; that is, repeated stimulus presentation diminishes or abolishes the response. In the present study, responses to auditory stimulation were found to be relatively localized to the area of the IVulst and its borders. Responses in the chicken further differ from those reported in reptilian general cortex in that they are of shorter latency (5-14 msec) and are not easily habituated. Responses to visual stimulation in the chicken show a diffuseness and a lack of localization similar to those found in the reptile, but these are again of shorter latency (IO-20 msec) and are not susceptible to habituation. Further, the insensitivity of the visually evoked activity to surface procainization and its constant characteristics at differing depths suggest that the source of this activity is not on the surface of the telencephalon or within the immediately subjacent lamellae. Unlike responses recorded from primary sensory areas of mammalian neocortex, auditory and visual stimuli do not evoke responses in discrete areas of the Wulst. However, variations between avian responses evoked by sensory stimulation (auditory and visual) and reptilian responses obtained from similar stimuli indicate that the avian Wulst is functionally different than mammalian primary sensory neocortes. and reptilian nonspecific general cortex. Tactile stimulation was not found to elicit responses from any point on the telencephalic surface: although one area of response was found at a depth suggestive of ventral hyperstriatum or neostriatum. This is in agreement with Gogan (2) who reported responses to tactile stimulation from polysensory units in these areas in the pigeon. Erulkar (1) recorded responses to auditory as well as tactile stimulation only from the neostriatum caudale (pigeon) and not from the hyperstriatum. Spooner and ffinters (6 ) reported that in unanesthetized chicks, the responses to both auditory and visual stimulation were much more widespread than in birds even lightly anesthetized with barbiturates, and that the auditory responses are particularly depressed by this anesthetic. .\lthouph there is always the possibility of a species difference between the pigeon and the chicken, it seems reasonable to suppose that the use of chloralose rather than barbiturates in the present
SO4
ADAM0
AND
KING
study may account for the finding of auditory responses at higher telencephalic levels than those reported by Erulkar. The presence of these responses suggests that in the chicken, cells in the area of the \Vulst are involved in the auditory projection system. ?Horeover, the characteristics of the response indicate that these cells are located fairly close to the telencephalic surface, probably within the most superficial 350-400 IL, an area which would comprise the superficial corticoid layer and the accessory hyperstriatum. These findings indicate the presence of auditory connections in structures above the neostriatum; and in at least part of the system. these auditory connections are mediated not through diffuse polysensory and highly complex pathways, but by a more direct route containing relatively few synapses. References 1. 2. 3.
4. 5. 6.
ERULKAR, S. D. 1955. Tactile and auditory areas in the brain of the pigeon. .4n experimental study by means of evoked potentials. J. Contp. Nezrrol. 103: 420-457. GOCAN, P. 1963. Projections sensorielles au niveau du telencephalechez le pigeon saris anesthesie generale. J. Physiol. Paris 55: 258-259. KAPPERS, C. U. .a., G. C. HUBER, and E. C. CROSBY. 1936. “The Comparative Anatomy of the Nervous Systems of Vertebrates, Including Man,” 1: 467-484. Macmillan, New York. MOORE, G. P., and R. D. TSCHIRGI. 1962. Nonspecific responses of reptilian cortex to sensory stimuli. Exptl. Neural. 5: 196-209. ROWXUL, L. .I. 1957. “Explorations oscillographique de la voie visuelle du Pigeon.” Fouloun. Paris. (Thesis.) SPOONER. C. E., and W. D. WINTERS. 1965. Distribution of auditory and visual evoked responses in the central nervous system of the unanesthetized chick. Physiologist 8: 279.
Evoked
KEUROLOGY
17,
495-504
Responses Auditory, NORMA
in the Visual,
Chicken
and
Tactile
Telencephalon
to
Stimulation
ADAMO AND ROBERT L. KING’
JEAN
Departments of Anatomy U&ersity of Florida
(1967)
and
Physiology and Center for Neurobiological Sciences, College of Medicine, Gainesville, Florida 32603
Received
December
22. 1966
Auditory, visual and cutaneous electrical stimulations were administered to anesthetized chickens and the evoked responses to each stimulus modality was systematically recorded from the cerebral hemispheres. Principal responses to auditory stimulation were observed predominantly from the Wulst (dorsomedial sagittal elevation of the avian forebrain). Application of 1% procaine to the surface of the Wulst either decreased or abolished the response, indicating that the Wulst has a functional anatomical role in the chicken’s auditory system. Responses to photic stimulation also were recorded from the Wulst and surrounding hemispheric areas. Since topical application of 1% procaine to the cerebral hemispheres did not alter the visually evoked responses, forebrain structures responsible for these responses are thought to be in areas other than the Wulst. Cutaneous electrical stimulation was not found to produce responses from the Wulst or surrounding hemispheric areas. The characteristics of the responses obtained in birds to auditory stimulation are compared to those reported for the alligalor. The differences found suggest that the avian Wulst functions differently from the reptilian “general cortex” with respect to the auditory system. The present observations in birds are interpreted to indicate that the Wulst is related to the auditory system by fiber connections which have relatively few synapses. Introduction
Direct anatomical evidence for termination of the auditory, visual and tactile systems in the avian forebrain has yet to be unequivocally established. From an extensive electrophysiological study of auditory and tactile relays in the pigeon, Erulkar (1) was able to determine that certain regions of the brain stem and cerebral hemispheres were activated by tactile and auditory stimulation. Both stimulus modalities were found to evoke responses from discrete areas in the neostriatum caudale, but not from the hyperstriatum. 1 This work was supported Blindness, National Institutes of received support from Training Henry R. Wilson for his help Dept. of Anatomy, University Mexico 87106.
by the National Institute of Neurological Diseases and Health, under Grants NB-3990 and NB-1548. Dr. Adamo Grant Z-TIGM-579. The authors are indebted to Dr. in supplying animals. Dr. Adamo’s present address is: of New Mexico School of Medicine, Albuquerque, New
498
CHICKEN
TELENCEPH.ALON
499
Rougeul (S), also working with pigeons, presented evidence that visual stimulation activates areas of the forebrain immediately below the \Yulst (dorsomedial sagittal elevation of the avian forebrain). Gogan (2) found polysensory units in the pigeon telencephalon which were responsive to light, sound and somesthetic stimulation; the location of these polysensory units were not indicated. The present study was undertaken to determine if the Wulst may participate as a functional anatomical component in the auditory. visual and tactile systems in the chicken. Materials
and
Methods
Thirty-nine adult chickens between the ages of 12 and 20 weeks were used in this study. Chloralose anesthesia (100 mg kg) was administered intramuscularly and gallamine triethiodide (3-5 mg,, kg, im or iv) was given as needed for immobilization. The birds were maintained on artificial respiration and their heads fixed in position. The hemispheres were exposed and the Wulst and surrounding hemispheric areas explored monopolarly with KClfilled capillary microelectrodes with 3-5 p diameter tips. Amplification was through an a-c coupled amplifier system with cathode follower. .L\ll responses were observed on a dual beam cathode ray oscilloscope and many cases were averaged by a (CAT) computer before permanent recordings were made photographically. Auditory stimuli were produced by feedin g O.l-msec square waves into a speaker. The resulting clicks were delivered at 4-set intervals to the left ear through a plastic tube leading from the speaker to the bird’s ear. Xo attempt was made to seal off or deafen the right ear; therefore it is assumed that stimulation was to some extent bilateral. Single Aash photic stimuli were given simultaneously to both eyes with a pulsed strobe light at a distance of approximately 45.5 cm. Single shock cutaneous stimuli (approsimately lol.Sv, 1-msec duration) were delivered through closely spaced needle electrodes placed at numerous positions on the body surface. Results
The Wulst is a three-layered elevated area on the dorsomedial surface of the avian neopallium. It contains the accessory hyperstriatum (immediately subjacent to the superficial corticoid layer), the dorsal hyperstriatum (deepest of the three layers), and the nucleus intercalatus (situated between the accessory and dorsal hyperstriata). Immediately below the Wulst is the ventral hyperstriatum (Fig. 1). Externally, the \Vulst is separated from the remainder of the hemisphere by a fissure, the vallecula. The majority of the electrode points explored in and around the U’ulst were tested with auditory (click), photic, and cutaneous electrical stimulation. Responses evoked by click stimulation were primarily surface positive.
500
ADAM0
AND
KING
FIG. 1. Sagittal section through the chicken hyperstriatum; X.1., nucleus intercalatus; D.H., hyperstriatum; S, neostriatum; P, paleostriatum; Wulst consists of the accessory hyperstriatum, the intercalatus.
brain. -4bbreviations: .4.H.. accessor dorsal hyperstriatum; V.H.. ventral .4, archistriatum; V, ventricle. The dorsal hyperstriatum, and the nucleus
consisting of either a single positive component followed by a small negative slow wave, or of a group of two to three brief positive-negative components, again followed by a small negative slow wave. Most of the responsesobserved were of the former type (Fig. 2, left). Latencies of the majority of the responsesrecorded from the Wulst were in the range of 5-8 msec though a few responses,mainly from caudal areas,had latenciesaslong as 14 msec.Duration of the auditory responseswas usually about 20 msec. At the caudal boundary of the Wulst, an occasional responsewas recorded which showed a much more pronounced surface negativity. These responseswere longer in latency (14-20 msec) with a negative component lasting for approximately 40 msec. The few responsesto click stimulation obtained outside the Wulst were of smaller amplitude than those found within the Wulst, and were much less reliably present. Responsesof this kind were found in the only hemispheric area immediately caudal to the Wulst. Responsesto photic stimulation were found throughout the hemispheres. Such responseswere of longer latency (IO-20 msec), longer duration (up to 150 msec), and larger amplitude than the responsesobtained with auditory stimulation. Photic responsestypically exhibited an initial surface negativity, followed by a longer lasting positive-negative complex (Fig. 2, right ). Activation of the telencephalon by cutaneous electrical stimulation was found in only one electrode tract, and that only at a depth of 3200 p (below the Wulst proper, and probably in the neostriatum). The remainder
CHICKEN
TELENCEPHALON
F1c:. _. 3 Left column: Evoked responses t\veen pulses, .5 msec; calibration, 100 kv. Cup~wr) and acoustic (middle1 stimulation;
in \Vulst to acoustic stimulation; Right column: Evoked rcsponscs calibration, 100 !LV.
SO1
time beto photic
of the hemispheric surface and its underlying structures were found to show responses only to auditory and photic stimulation. Responses exhibiting initially surface-positive activity to auditory stimulation and initially surface-negative activity to photic stimulation were recorded from identical points in the area of the R’ulst. Depth recording typically showed a decrease in amplitude of the auditory responses at 200-300 11sometimes, though rarely, associated with a reversal to initial negativity. Below this level the initial positivity returned, with a decrease in the succeeding negative wave until a point (about 2 800 10 was reached below the level of the L\‘ulst proper (Fig. 3)! Application to the surface of the LVulst of small bits of filter paper soaked in lc/r procaine solution decreased or abolished the surface response to auditory stimulation, indicating that the superficial layers are active in auditory function. Following application of 17; procaine responses to photic stimulation were not affected in any way, suggesting that these responses have their origin somewhere in deeper structures of the forebrain.
502
ADAM0
AND
depths
through
KING
SURF
200 400
800
1200 1.600
2000
2400
2800 3200
3600
4000
FIG.
CAT
3. Responses at varyinp computer for one trace).
the
Wulst
(25
responses
averaged
by
CHICKEN
TELENCEPH.ALOS
503
Discussion
As far rostrally as the auditory pathways have been histologically determined, the available morphological data indicate that the afferent systems of birds and reptiles are almost identical. However. electro-anatomical studies by Moore and Tschirgi (4) show that in the reptile (alligator) telencephalon. visual, auditory and tactile stimulation will elicit responses bilaterally and diffusely throughout the “general cortex” described by Kappers, Huber and Crosby (3). These polysensory responses have long latencies (SO-100 msec) and become rapidly attenuated or habituated; that is, repeated stimulus presentation diminishes or abolishes the response. In the present study, responses to auditory stimulation were found to be relatively localized to the area of the IVulst and its borders. Responses in the chicken further differ from those reported in reptilian general cortex in that they are of shorter latency (5-14 msec) and are not easily habituated. Responses to visual stimulation in the chicken show a diffuseness and a lack of localization similar to those found in the reptile, but these are again of shorter latency (IO-20 msec) and are not susceptible to habituation. Further, the insensitivity of the visually evoked activity to surface procainization and its constant characteristics at differing depths suggest that the source of this activity is not on the surface of the telencephalon or within the immediately subjacent lamellae. Unlike responses recorded from primary sensory areas of mammalian neocortex, auditory and visual stimuli do not evoke responses in discrete areas of the Wulst. However, variations between avian responses evoked by sensory stimulation (auditory and visual) and reptilian responses obtained from similar stimuli indicate that the avian Wulst is functionally different than mammalian primary sensory neocortes. and reptilian nonspecific general cortex. Tactile stimulation was not found to elicit responses from any point on the telencephalic surface: although one area of response was found at a depth suggestive of ventral hyperstriatum or neostriatum. This is in agreement with Gogan (2) who reported responses to tactile stimulation from polysensory units in these areas in the pigeon. Erulkar (1) recorded responses to auditory as well as tactile stimulation only from the neostriatum caudale (pigeon) and not from the hyperstriatum. Spooner and ffinters (6 ) reported that in unanesthetized chicks, the responses to both auditory and visual stimulation were much more widespread than in birds even lightly anesthetized with barbiturates, and that the auditory responses are particularly depressed by this anesthetic. .\lthouph there is always the possibility of a species difference between the pigeon and the chicken, it seems reasonable to suppose that the use of chloralose rather than barbiturates in the present
SO4
ADAM0
AND
KING
study may account for the finding of auditory responses at higher telencephalic levels than those reported by Erulkar. The presence of these responses suggests that in the chicken, cells in the area of the \Vulst are involved in the auditory projection system. ?Horeover, the characteristics of the response indicate that these cells are located fairly close to the telencephalic surface, probably within the most superficial 350-400 IL, an area which would comprise the superficial corticoid layer and the accessory hyperstriatum. These findings indicate the presence of auditory connections in structures above the neostriatum; and in at least part of the system. these auditory connections are mediated not through diffuse polysensory and highly complex pathways, but by a more direct route containing relatively few synapses. References 1. 2. 3.
4. 5. 6.
ERULKAR, S. D. 1955. Tactile and auditory areas in the brain of the pigeon. .4n experimental study by means of evoked potentials. J. Contp. Nezrrol. 103: 420-457. GOCAN, P. 1963. Projections sensorielles au niveau du telencephalechez le pigeon saris anesthesie generale. J. Physiol. Paris 55: 258-259. KAPPERS, C. U. .a., G. C. HUBER, and E. C. CROSBY. 1936. “The Comparative Anatomy of the Nervous Systems of Vertebrates, Including Man,” 1: 467-484. Macmillan, New York. MOORE, G. P., and R. D. TSCHIRGI. 1962. Nonspecific responses of reptilian cortex to sensory stimuli. Exptl. Neural. 5: 196-209. ROWXUL, L. .I. 1957. “Explorations oscillographique de la voie visuelle du Pigeon.” Fouloun. Paris. (Thesis.) SPOONER. C. E., and W. D. WINTERS. 1965. Distribution of auditory and visual evoked responses in the central nervous system of the unanesthetized chick. Physiologist 8: 279.