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Representation of the cochlea in primary auditory cortex of the ferret (Mustela putorius)
111
Hearing Research, 24 (1986) 111-115
Elsevier HRR 00813
Representation of the cochlea in primary auditory cortex of the ferret
( Mustela putorius
)
Jack B. Kelly, Peter W. Judge and Dennis P. Phillips * Department of Psychology, Carleton University, Ottawa, Ontario, KIS 5B6 Canada
(Received 27 January 1986; accepted 22 April 1986)
In seven barbiturate-anesthetized ferrets, we explored the acousticalfy sensitive cortex with conventional microelectrode mapping techniques. A tonotopically organized field was found whose orientation was such that high tonal frequencies were represented dorsally, and low frequencies ventrally. Within this field, neurons typically had short (12-20 ms) latent periods to first spikes. In conjunction with extant anatomical evidence on the connectivity of this region, these data suggest that this field represents the ferret’s primary auditory cortex. ferret, auditory cortex. tonotopic organization
Introduction
The ferret is a highly altricial carnivore with relatively late development of auditory function. Both physiological (inferior colliculus) and behavioral responses to sound are first seen around 32 days after birth, as compared to a few days after birth in the cat (Moore, 1982). For this reason, the ferret represents an opportune species in which to examine the developing mammalian auditory system. In addition, the adult ferret is readily trained in a variety of behavioral tasks, and has been used to advantage in studies of the effects of cortical lesions on sound localization (Kavanagh and Kelly, 1983, ~npubl.). With these ~nsiderations in mind, we have examined some general features of the normal adult ferret’s primary auditory cortex using conventional neurophysiological mapping techniques (Merzenich and Brugge, 1973; Merzenich et al., 1975; Reale and Imig, 1980). The experiments provided data on the organization of the ferret’s auditory cortex, which suggest that this species has a cortical auditory area particularly suitable for studies of cortical development or further behavioral lesion studies. * Presentaddress: Department of Psychology, Dalhousie University, Halifax, Nova Scotia, B3H 451 Canada. 0378-5955/86/$03.50
Two independent lines of evidence from Kavanagh and Kelly (unpubl.) led us to believe that the ferret’s primary auditory cortex is located on the gyrus bounded by the acute angle of this species’ suprasylvian sulcus. First, injections of horseradish peroxidase into this cortical locus (the middle ectosylvian gyrus) result in dense retrograde labelling of the laminated ventral nucleus of the thalamic medial geniculate body, while lesion of this cortical site results in profound retrograde cell degeneration of the same thalamic nucleus. Horseradish peroxidase injections restricted to the more ventrally located anterior and posterior ectosylvian gyri result in labelling predo~nantly within the magn~llul~ division of the medial geniculate or the posterior thalamic group (PO). Second, unilateral ablation of the middle ectosylvian gyrus results in severe and permanent loss of sound localization ability for sources in the contralateral acoustic hemifield, a deficit which is associated with primary auditory cortical lesions in the cat (Jenkins and Merzenich, 1984). Materials and Methods
Data were obtained from 7 adult ferrets with infection-free ears. Surgical anesthesia was induced with sodium pentobarbital (35 mg/kg i.p.)
0 1986 Elsevier Science Publishers B.V. (Biomedi~l Division)
and was supplemented with additional doses administered to maintain a state of areflexia. Three of these ferrets additionally received dexamethasone sodium phosphate (0.05 mg/kg i.m.) as a prophylactic against cerebral edema. Briefly, the surgical preparation for acute experiments entailed resection of the left temporal musculature, and exposure of the left middle ectosylvian gyrus by removal of the overlying bone and reflection of the dura mater. The cortex was continuously bathed in warmed dimethylpolysiloxane oil. Tone pulses of 100 ms duration, including 5 ms rise-decay times, were presented at l/s and transduced by KEF high frequency (Type SP1032) and midrange (Type AD5060) speakers in a crossover network located 16 inches from the contralateral pinna. Measurements of tone intensity in dB SPL (sound pressure level: dB re 20 uPa) obtained using a Bri.iel & Kjaer 0.5 inch condenser microphone in place of the ferret revealed that the maximum output of the stimulating system rose from 67 dB at 50 Hz to 114 dB at 400. Hz, declined to 102 dB at 2 kHz, and with the exception of a single, 20 dB-steep, 300 Hz-wide trough centered at 7.1 kHz, was 1-6 dB to 32.0 kHz. The ferret was located in a sound-attenuating room. The responses of single neurons or neuron clusters were recorded extra-cellularly using insulated tungsten microelectrodes (1.1-1.5 MO at 1 kHz) that were usually advanced into the cortex perpendicular to the pial surface. When a neuron or cluster of neurons was isolated, its threshold CF (characteristic frequency: the tone frequency for which the neural elements had their lowest excitatory SPL) was determined audiovisually. The CF tone threshold was recorded, and minimum response latencies for suprathreshold CF tones were obtained by reading first-spike times from a stimulus-triggered oscilloscope. Latencies reported here include an approximately 1.2 ms propagation time from the loudspeaker. Penetration sites were marked in relation to cerebrovascular landmarks on a working Polaroid print. In the barbiturate-anesthetized ferret, an acoustically sensitive area of cortex was found within the tissue bounded by the suprasylvian sulcus and dorsocaudal to the single (‘Sylvian’) fissure which divides that region into anterior and posterior (‘ectosylvian’) gyri. Within this region,
including part of the ventral bank of the sylvian sulcus, neuron clusters were usually tuned to tone frequency and displayed defined CFs. In penetrations avoiding sulcal CFs were relatively constant with electrode within the cortex.
suprasharply clearly banks, depth
Results Fig. 1 presents schematic illustrations of this region in the two ferrets for which we obtained the most detailed maps of tonal sensitivity. In each case, the numbers indicate the CFs, expressed in kHz, of neurons or clusters at that recording site. In the instance of ferret no. 92 (Fig. lA), neurons of the highest recorded CF (near 25 kHz) were found at the most dorsal tip of the confluence of the ectosylvian gyri, and in the ventral bank of the suprasylvian sulcus into which it folds. Exploration of the crown of the ectosylvian gyrus revealed neuron clusters whose CFs fell as the electrode was placed more ventrally. An indication of the orderliness of this frequency representation is provided by the dashed lines which depict ‘isofrequency contours’ (lines of cells with similar CFs, after Merzenich et al., 1975). It is apparent that these contours are disposed in a roughly rostral-to-caudal plane, reflecting a systematic tonotopic axis in the dorsal-to-ventral plane across the cortex surface. In this, and other animals, the low frequency border of this tonotopic field blended more or less diffusely into a region that was either unresponsive to tonal stimuli (‘NR’ in Fig. 1) or which occasionally revealed broadly tuned elements (‘B’). In the instance of ferret no. 93 (Fig. lB), the cortical representation of very high tone frequencies was likely buried in the ventral bank of the suprasylvian sulcus, since study of the exposed crown of the ectosylvian gyrus revealed neuron clusters of low and medium CFs. As in the previous case, however, there was an orderly representation of tone frequency across the cortical surface. The isofrequency contours in this ferret’s cortex were closer to rostrodorsal-to-ventrocaudal in orientation than in ferret no. 92. The low frequency border of this tonotopically-mapped region again abutted a zone of cortex that was, for the most part, unresponsive to tones.
113
30-A
N=!37
i ‘l 20. 0
7 a POln
% n
FERRET
93
B N=104
80.
d 5 w 40.
.
..
.
.:. :
.
.
. . : . .
.
.
. : .
.. . ...
.
.
.
: ..,.
% t-
.: :. ‘:..
‘
..
: \
‘: .
.
:
.
.. ...‘I ‘.>’ *
Fig. 2. A. Distribution of minimum first spike latencies for neurons and neuron clusters recorded in ferrets no. 92 and no. 93. B. Distribution of CF thresholds, plotted as a function of CF, for recording sites in ferrets no. 92 and no. 93.
Fig. 1. A. Schematic depiction of the left auditory cortex of ferret no. 92. Thick lines represent sulci. Numbers represent CFs, expressed in kHz, of neuron clusters at indicated sites. Dashed lines represent isofrequency contours, i.e., lines of cells with similar or identical CFs. Note that there is an orderly progression of CFs across the cortex surface, with high frequencies being represented dorsally. Inset shows representative sulcal pattern of an adult ferret, with the cortical area mapped indicated by shading. B. Data for the left auditory cortex of ferret no. 93. Details as for A. Abbreviations: B, broadly tuned neurons with no clearly defined CF; NR, no response to tonal stimuli; SF, sylvian fissure; SSS, suprasylvian sulcus.
Minimum response latency data for CF tones were obtained from 97 recording sites in the two ferrets for which tonotopic maps were presented in Fig. 1. The distribution of latent period to first spike data are presented in Fig. 2A. Inspection of these data reveals that the vast majority of spike responses occurred within the range from 12 to 19 ms of stimulus onset. There was no systematic relationship between CF and minimum latent period. In the few instances in which latency data
were obtained from broadly tuned neurons (see Fig. l), latent periods were usually 5 to 10 ms longer. Threshold SPLs for CF tones were obtained from 104 recording sites in ferrets no. 92 and no. 93. These data must be qualified to the extent that acoustic calibrations were obtained by a substitution method (see above) which does not take into account the passive acoustic transmission properties of the external ear (Phillips et al., 1982) and which does not, therefore, specify tympanic SPLs precisely. On the other hand, these free field data enable direct comparisons with behavioral thresholds obtained under comparable free field conditions. Fig. 2B presents CF thresholds plotted as a function of CF for the 104 observations. A scrutiny of these data reveals that neurons of any given CF displayed a broad range of thresholds, with neurons whose CFs were between 5 and 13 kHz having the greatest absolute sensitivities. Similar findings have been reported for cells in the ferret’s inferior colliculus (Moore et al., 1983). This region of maximum sensitivity corresponds closely to estimates of best frequency obtained
114
from the behavioral audiogram in the same species (Kelly et al., 1986). Discussion
This report has presented preliminary evidence on the physiology of the ferret’s auditory cortex. In the zone of cortex previously found to receive dense projections from the ventral division of the medial geniculate body, and which, when lesioned unilaterally, results in profound sound localization deficits in the contralateral auditory hemifield (Kavanagh and Kelly, 1983, unpubl.), we found a tonotopically organized auditory field (Fig. 1). Although we have not explored the neighboring sulcal banks in detail, no clear reversals in tonotopic sequence in penetrations through the sulcal walls were apparent. This leaves open the question of whether the ferret, like the marsupial possum (Gates and Aitkin, 1982), has only one such cortical field, or whether further studies might reveal additional tonotopic fields as in the cat (Knight, 1977; Merzenich et al., 1975; Reale and Imig, 1980; Phillips and Irvine, 1982; Imig and Morel, 1983; Phillips and Orman, 1984). The minimum first spike latencies for neurons within this field (Fig. 2A) are comparable to those presented for the cat’s primary auditory cortex (P~llips et al., 1985), and the correspondence between behavioral and cortical neural ‘audiograms’ is also common to the cat’s primary field (Phillips and Irvine, 1981). Taken together, these data suggest that the tonotopically organized field described in this report represents the ferret’s primary auditory cortex. The tonotopic organization of the primary auditory cortex has been described in a broad range of species. In cats (Merzenich et al., 1975; Reale and Imig, 1980) and monkeys (Merzenich and Brugge, 1973; Irnig et al., 1977; Brugge, 1982), the topography of this field is such that high tonal frequencies are represented rostrally, and low frequencies caudally. The reverse pattern is found in the grey squirrel (Merzenich et al., 1976) and guinea pig (Hellweg et al., 1977). In the ferret, we found the tonotopic axis to lie in an intermediate plane, viz., roughly dorso-ventral, with high frequencies being respresented dorsally. This pattern is comparable to that described for the rabbit (McMullen and Glaser, 1982) and marsupial pos-
sum (Gates and Aitkin, 1982). The fact that the ferret’s primary field is located on the crown of a gyrus to which access is readily obtained through the lateral skull suggests that it may be a suitable model system for the behavioral consequences of focal lesions of physiologically characterized loci. Acknowledgements We express our special thanks to Karyn Boak for her technical assistance throughout these experiments. This research was supported by NSERC Grants Nos. 7654 to J.B.K. and U0442 to D.P.P. References Brugge, J.F. (1982): Auditory cortical areas in primates. In: Cortical Sensory Organization, Volume 3, Multiple Auditory Areas, pp. 59-70. Editor: C.N. Woolsey. Humana Press, Clifton, NJ. Gates, G.R. and Aitkin, L.M. (1982): Auditory cortex in the marsupial possum (Trichosurus vulpecula). Hearing Res. I, l-11. Hellweg, F.C., Koch, R. and Vollrath, M. (1977): Representation of the cochlea in the neocortex of the guinea pig. Exp. Brain Res. 29, 467-474. lmig, T.J. and Morel, A. (1983): Organization of the thalamocortical auditory system in the cat. Annu. Rev. Neurosci. 6, 95-120. lmig, T.J., Ruggero, M.A., Kitzes, L.M., Javel, E. and Brugge, J.F. (1977): ~ga~zation of auditory cortex in the owl monkey (Aotus triuirgatw). J. Comp. Neurol. 171, X11-128. Jenkins, W.M. and Merzenich, M.M. (1984): Role of cat primary auditory cortex for sound localization behavior. J. Neurophysiol. 52, 819-847. Kavanagh, G.L. and Kelly, J.B. (1983): The effects of auditory cortical lesions on seven-choice sound localization by ferrets. Sot. Neurosci. Abstr. 9, 956. Kavanagh, G.L. and Kelly, J.B. (unpubl.): Contribution of auditory cortex to sound localization by the ferret (Musrela putorius). Kelly, J.B.. Kavanagh, G.L. and Dalton. J.C.H. (1986f: Hearing in the ferret (Mustela putoriw): thresholds for pure tone detection. Unpublished manuscript. Knight, P.L. (1977): Representation of the cochlea within the anterior auditory field (AAF) of the cat. Brain Res. 130, 447-467. McMullen, N.T. and Glaser, E.M. (1982): Tonotopic organization of rabbit auditory cortex. Expl. Neurol. 75, 208-220. Merzenich, M.M. and Brugge, J.F. (1973): Representation of the cochlear partition on the superior temporal plane of the macaque monkey. Brain Res. SO, 275-296. Merzenich, M.M., Knight. P.L. and Roth, G.L. (1975): Representation of cochlea within primary auditory cortex in the cat. J. Neurophysiol. 38, 237-249. Merzenich, M.M., Kaas, J.H. and Roth, G.L. (1976): Auditory
115
cortex in the grey squirrel: tonotopic organization and architectonic fields. J. Comp. Neurol. 166, 387-402. Moore, D.R. (1982): Late onset of hearing in the ferret. Brain Res. 253, 309-311. Moore, D.R., Semple, M.N. and Addison, P.D. (1983): Some acoustic properties of neurones in the ferret inferior colliculus. Brain Res. 269, 69-82. Phillips, D.P. and Irvine, D.R.F. (1981): Responses of single neurons in physiologically defined primary auditory cortex (AI) of the cat: frequency tuning and responses to intensity. J. Neurophysiol. 45, 48-58. Phillips, D.P. and Irvine, D.R.F. (1982): Properties of neurons in AAF of cat cerebral cortex. Brain Res. 248, 237-244.
Phillips, D.P. and Orman, S.S. (1984): Responses of single neurons in posterior field of cat auditory cortex to tonal stimulation. J. Neurophysiol. 51, 147-163. Phillips, D.P., Calford, M.B., Pettigrew, J.D., Aitkin, L.M. and Semple, M.N. (1982): Directionality of sound pressure transformation at the cat’s pinna. Hearing Res. 8, 13-28. Phillips, D.P., Orman, S.S., Musicant, A.D. and Wilson, G.F. (1985): Neurons in the cat’s primary auditory cortex distinguished by their responses to tones and wide-spectrum noise. Hearing Res. 18, 73-86. Reale, R.A. and Imig, T.J. (1980): Tonotopic organization in auditory cortex of the cat. J. Comp. Neurol. 192, 265-291.
Hearing Research, 24 (1986) 111-115
Elsevier HRR 00813
Representation of the cochlea in primary auditory cortex of the ferret
( Mustela putorius
)
Jack B. Kelly, Peter W. Judge and Dennis P. Phillips * Department of Psychology, Carleton University, Ottawa, Ontario, KIS 5B6 Canada
(Received 27 January 1986; accepted 22 April 1986)
In seven barbiturate-anesthetized ferrets, we explored the acousticalfy sensitive cortex with conventional microelectrode mapping techniques. A tonotopically organized field was found whose orientation was such that high tonal frequencies were represented dorsally, and low frequencies ventrally. Within this field, neurons typically had short (12-20 ms) latent periods to first spikes. In conjunction with extant anatomical evidence on the connectivity of this region, these data suggest that this field represents the ferret’s primary auditory cortex. ferret, auditory cortex. tonotopic organization
Introduction
The ferret is a highly altricial carnivore with relatively late development of auditory function. Both physiological (inferior colliculus) and behavioral responses to sound are first seen around 32 days after birth, as compared to a few days after birth in the cat (Moore, 1982). For this reason, the ferret represents an opportune species in which to examine the developing mammalian auditory system. In addition, the adult ferret is readily trained in a variety of behavioral tasks, and has been used to advantage in studies of the effects of cortical lesions on sound localization (Kavanagh and Kelly, 1983, ~npubl.). With these ~nsiderations in mind, we have examined some general features of the normal adult ferret’s primary auditory cortex using conventional neurophysiological mapping techniques (Merzenich and Brugge, 1973; Merzenich et al., 1975; Reale and Imig, 1980). The experiments provided data on the organization of the ferret’s auditory cortex, which suggest that this species has a cortical auditory area particularly suitable for studies of cortical development or further behavioral lesion studies. * Presentaddress: Department of Psychology, Dalhousie University, Halifax, Nova Scotia, B3H 451 Canada. 0378-5955/86/$03.50
Two independent lines of evidence from Kavanagh and Kelly (unpubl.) led us to believe that the ferret’s primary auditory cortex is located on the gyrus bounded by the acute angle of this species’ suprasylvian sulcus. First, injections of horseradish peroxidase into this cortical locus (the middle ectosylvian gyrus) result in dense retrograde labelling of the laminated ventral nucleus of the thalamic medial geniculate body, while lesion of this cortical site results in profound retrograde cell degeneration of the same thalamic nucleus. Horseradish peroxidase injections restricted to the more ventrally located anterior and posterior ectosylvian gyri result in labelling predo~nantly within the magn~llul~ division of the medial geniculate or the posterior thalamic group (PO). Second, unilateral ablation of the middle ectosylvian gyrus results in severe and permanent loss of sound localization ability for sources in the contralateral acoustic hemifield, a deficit which is associated with primary auditory cortical lesions in the cat (Jenkins and Merzenich, 1984). Materials and Methods
Data were obtained from 7 adult ferrets with infection-free ears. Surgical anesthesia was induced with sodium pentobarbital (35 mg/kg i.p.)
0 1986 Elsevier Science Publishers B.V. (Biomedi~l Division)
and was supplemented with additional doses administered to maintain a state of areflexia. Three of these ferrets additionally received dexamethasone sodium phosphate (0.05 mg/kg i.m.) as a prophylactic against cerebral edema. Briefly, the surgical preparation for acute experiments entailed resection of the left temporal musculature, and exposure of the left middle ectosylvian gyrus by removal of the overlying bone and reflection of the dura mater. The cortex was continuously bathed in warmed dimethylpolysiloxane oil. Tone pulses of 100 ms duration, including 5 ms rise-decay times, were presented at l/s and transduced by KEF high frequency (Type SP1032) and midrange (Type AD5060) speakers in a crossover network located 16 inches from the contralateral pinna. Measurements of tone intensity in dB SPL (sound pressure level: dB re 20 uPa) obtained using a Bri.iel & Kjaer 0.5 inch condenser microphone in place of the ferret revealed that the maximum output of the stimulating system rose from 67 dB at 50 Hz to 114 dB at 400. Hz, declined to 102 dB at 2 kHz, and with the exception of a single, 20 dB-steep, 300 Hz-wide trough centered at 7.1 kHz, was 1-6 dB to 32.0 kHz. The ferret was located in a sound-attenuating room. The responses of single neurons or neuron clusters were recorded extra-cellularly using insulated tungsten microelectrodes (1.1-1.5 MO at 1 kHz) that were usually advanced into the cortex perpendicular to the pial surface. When a neuron or cluster of neurons was isolated, its threshold CF (characteristic frequency: the tone frequency for which the neural elements had their lowest excitatory SPL) was determined audiovisually. The CF tone threshold was recorded, and minimum response latencies for suprathreshold CF tones were obtained by reading first-spike times from a stimulus-triggered oscilloscope. Latencies reported here include an approximately 1.2 ms propagation time from the loudspeaker. Penetration sites were marked in relation to cerebrovascular landmarks on a working Polaroid print. In the barbiturate-anesthetized ferret, an acoustically sensitive area of cortex was found within the tissue bounded by the suprasylvian sulcus and dorsocaudal to the single (‘Sylvian’) fissure which divides that region into anterior and posterior (‘ectosylvian’) gyri. Within this region,
including part of the ventral bank of the sylvian sulcus, neuron clusters were usually tuned to tone frequency and displayed defined CFs. In penetrations avoiding sulcal CFs were relatively constant with electrode within the cortex.
suprasharply clearly banks, depth
Results Fig. 1 presents schematic illustrations of this region in the two ferrets for which we obtained the most detailed maps of tonal sensitivity. In each case, the numbers indicate the CFs, expressed in kHz, of neurons or clusters at that recording site. In the instance of ferret no. 92 (Fig. lA), neurons of the highest recorded CF (near 25 kHz) were found at the most dorsal tip of the confluence of the ectosylvian gyri, and in the ventral bank of the suprasylvian sulcus into which it folds. Exploration of the crown of the ectosylvian gyrus revealed neuron clusters whose CFs fell as the electrode was placed more ventrally. An indication of the orderliness of this frequency representation is provided by the dashed lines which depict ‘isofrequency contours’ (lines of cells with similar CFs, after Merzenich et al., 1975). It is apparent that these contours are disposed in a roughly rostral-to-caudal plane, reflecting a systematic tonotopic axis in the dorsal-to-ventral plane across the cortex surface. In this, and other animals, the low frequency border of this tonotopic field blended more or less diffusely into a region that was either unresponsive to tonal stimuli (‘NR’ in Fig. 1) or which occasionally revealed broadly tuned elements (‘B’). In the instance of ferret no. 93 (Fig. lB), the cortical representation of very high tone frequencies was likely buried in the ventral bank of the suprasylvian sulcus, since study of the exposed crown of the ectosylvian gyrus revealed neuron clusters of low and medium CFs. As in the previous case, however, there was an orderly representation of tone frequency across the cortical surface. The isofrequency contours in this ferret’s cortex were closer to rostrodorsal-to-ventrocaudal in orientation than in ferret no. 92. The low frequency border of this tonotopically-mapped region again abutted a zone of cortex that was, for the most part, unresponsive to tones.
113
30-A
N=!37
i ‘l 20. 0
7 a POln
% n
FERRET
93
B N=104
80.
d 5 w 40.
.
..
.
.:. :
.
.
. . : . .
.
.
. : .
.. . ...
.
.
.
: ..,.
% t-
.: :. ‘:..
‘
..
: \
‘: .
.
:
.
.. ...‘I ‘.>’ *
Fig. 2. A. Distribution of minimum first spike latencies for neurons and neuron clusters recorded in ferrets no. 92 and no. 93. B. Distribution of CF thresholds, plotted as a function of CF, for recording sites in ferrets no. 92 and no. 93.
Fig. 1. A. Schematic depiction of the left auditory cortex of ferret no. 92. Thick lines represent sulci. Numbers represent CFs, expressed in kHz, of neuron clusters at indicated sites. Dashed lines represent isofrequency contours, i.e., lines of cells with similar or identical CFs. Note that there is an orderly progression of CFs across the cortex surface, with high frequencies being represented dorsally. Inset shows representative sulcal pattern of an adult ferret, with the cortical area mapped indicated by shading. B. Data for the left auditory cortex of ferret no. 93. Details as for A. Abbreviations: B, broadly tuned neurons with no clearly defined CF; NR, no response to tonal stimuli; SF, sylvian fissure; SSS, suprasylvian sulcus.
Minimum response latency data for CF tones were obtained from 97 recording sites in the two ferrets for which tonotopic maps were presented in Fig. 1. The distribution of latent period to first spike data are presented in Fig. 2A. Inspection of these data reveals that the vast majority of spike responses occurred within the range from 12 to 19 ms of stimulus onset. There was no systematic relationship between CF and minimum latent period. In the few instances in which latency data
were obtained from broadly tuned neurons (see Fig. l), latent periods were usually 5 to 10 ms longer. Threshold SPLs for CF tones were obtained from 104 recording sites in ferrets no. 92 and no. 93. These data must be qualified to the extent that acoustic calibrations were obtained by a substitution method (see above) which does not take into account the passive acoustic transmission properties of the external ear (Phillips et al., 1982) and which does not, therefore, specify tympanic SPLs precisely. On the other hand, these free field data enable direct comparisons with behavioral thresholds obtained under comparable free field conditions. Fig. 2B presents CF thresholds plotted as a function of CF for the 104 observations. A scrutiny of these data reveals that neurons of any given CF displayed a broad range of thresholds, with neurons whose CFs were between 5 and 13 kHz having the greatest absolute sensitivities. Similar findings have been reported for cells in the ferret’s inferior colliculus (Moore et al., 1983). This region of maximum sensitivity corresponds closely to estimates of best frequency obtained
114
from the behavioral audiogram in the same species (Kelly et al., 1986). Discussion
This report has presented preliminary evidence on the physiology of the ferret’s auditory cortex. In the zone of cortex previously found to receive dense projections from the ventral division of the medial geniculate body, and which, when lesioned unilaterally, results in profound sound localization deficits in the contralateral auditory hemifield (Kavanagh and Kelly, 1983, unpubl.), we found a tonotopically organized auditory field (Fig. 1). Although we have not explored the neighboring sulcal banks in detail, no clear reversals in tonotopic sequence in penetrations through the sulcal walls were apparent. This leaves open the question of whether the ferret, like the marsupial possum (Gates and Aitkin, 1982), has only one such cortical field, or whether further studies might reveal additional tonotopic fields as in the cat (Knight, 1977; Merzenich et al., 1975; Reale and Imig, 1980; Phillips and Irvine, 1982; Imig and Morel, 1983; Phillips and Orman, 1984). The minimum first spike latencies for neurons within this field (Fig. 2A) are comparable to those presented for the cat’s primary auditory cortex (P~llips et al., 1985), and the correspondence between behavioral and cortical neural ‘audiograms’ is also common to the cat’s primary field (Phillips and Irvine, 1981). Taken together, these data suggest that the tonotopically organized field described in this report represents the ferret’s primary auditory cortex. The tonotopic organization of the primary auditory cortex has been described in a broad range of species. In cats (Merzenich et al., 1975; Reale and Imig, 1980) and monkeys (Merzenich and Brugge, 1973; Irnig et al., 1977; Brugge, 1982), the topography of this field is such that high tonal frequencies are represented rostrally, and low frequencies caudally. The reverse pattern is found in the grey squirrel (Merzenich et al., 1976) and guinea pig (Hellweg et al., 1977). In the ferret, we found the tonotopic axis to lie in an intermediate plane, viz., roughly dorso-ventral, with high frequencies being respresented dorsally. This pattern is comparable to that described for the rabbit (McMullen and Glaser, 1982) and marsupial pos-
sum (Gates and Aitkin, 1982). The fact that the ferret’s primary field is located on the crown of a gyrus to which access is readily obtained through the lateral skull suggests that it may be a suitable model system for the behavioral consequences of focal lesions of physiologically characterized loci. Acknowledgements We express our special thanks to Karyn Boak for her technical assistance throughout these experiments. This research was supported by NSERC Grants Nos. 7654 to J.B.K. and U0442 to D.P.P. References Brugge, J.F. (1982): Auditory cortical areas in primates. In: Cortical Sensory Organization, Volume 3, Multiple Auditory Areas, pp. 59-70. Editor: C.N. Woolsey. Humana Press, Clifton, NJ. Gates, G.R. and Aitkin, L.M. (1982): Auditory cortex in the marsupial possum (Trichosurus vulpecula). Hearing Res. I, l-11. Hellweg, F.C., Koch, R. and Vollrath, M. (1977): Representation of the cochlea in the neocortex of the guinea pig. Exp. Brain Res. 29, 467-474. lmig, T.J. and Morel, A. (1983): Organization of the thalamocortical auditory system in the cat. Annu. Rev. Neurosci. 6, 95-120. lmig, T.J., Ruggero, M.A., Kitzes, L.M., Javel, E. and Brugge, J.F. (1977): ~ga~zation of auditory cortex in the owl monkey (Aotus triuirgatw). J. Comp. Neurol. 171, X11-128. Jenkins, W.M. and Merzenich, M.M. (1984): Role of cat primary auditory cortex for sound localization behavior. J. Neurophysiol. 52, 819-847. Kavanagh, G.L. and Kelly, J.B. (1983): The effects of auditory cortical lesions on seven-choice sound localization by ferrets. Sot. Neurosci. Abstr. 9, 956. Kavanagh, G.L. and Kelly, J.B. (unpubl.): Contribution of auditory cortex to sound localization by the ferret (Musrela putorius). Kelly, J.B.. Kavanagh, G.L. and Dalton. J.C.H. (1986f: Hearing in the ferret (Mustela putoriw): thresholds for pure tone detection. Unpublished manuscript. Knight, P.L. (1977): Representation of the cochlea within the anterior auditory field (AAF) of the cat. Brain Res. 130, 447-467. McMullen, N.T. and Glaser, E.M. (1982): Tonotopic organization of rabbit auditory cortex. Expl. Neurol. 75, 208-220. Merzenich, M.M. and Brugge, J.F. (1973): Representation of the cochlear partition on the superior temporal plane of the macaque monkey. Brain Res. SO, 275-296. Merzenich, M.M., Knight. P.L. and Roth, G.L. (1975): Representation of cochlea within primary auditory cortex in the cat. J. Neurophysiol. 38, 237-249. Merzenich, M.M., Kaas, J.H. and Roth, G.L. (1976): Auditory
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