RAPID COMMUNICATION
Somatosensory Input to Auditory Association Cortex in the
Macaque Monkey
CHARLES E. SCHROEDER,1–3 ROBERT W. LINDSLEY,1 COLLEEN SPECHT,1 ALVIN MARCOVICI,4
JOHN F. SMILEY,1 AND DANIEL C. JAVITT1,2,5
1
Cognitive Neuroscience and Schizophrenia Program, Nathan Kline Institute for Psychiatric Research, Orangeburg 10962;
2
Department of Neuroscience, 3Department of Neurology, and 4Department of Neurosurgery, Albert Einstein College of
Medicine, Bronx 10461; and 5Department of Psychiatry, New York University Medical Center, New York, New York 10003
Received 12 June 2000; accepted in final form 10 October 2000
Schroeder, Charles E., Robert W. Lindsley, Colleen Specht, Alvin
Marcovici, John F. Smiley, and Daniel C. Javitt. Somatosensory
input to auditory association cortex in the macaque monkey. J Neurophysiol 85: 1322–1327, 2001. We investigated the convergence of
somatosensory and auditory inputs in within subregions of macaque
auditory cortex. Laminar current source density and multiunit activity
profiles were sampled with linear array multielectrodes during penetrations of the posterior superior temporal plane in three macaque
monkeys. At each recording site, auditory responses to binaural clicks,
pure tones, and band-passed noise, all presented by earphones, were
compared with somatosensory responses evoked by contralateral median nerve stimulation. Subjects were awake but were not required to
discriminate the stimuli. Borders between A1 and surrounding belt
regions were identified by mapping best frequency and stimulus
preferences and by subsequent histological analysis. Regions immediately caudomedial to A1 had robust somatosensory responses corepresented with auditory responses. In these regions, both somatosensory and auditory response profiles had “feedforward” patterns;
initial excitation beginning in Lamina 4 and spreading to extragranular laminae. Auditory and somatosensory responses displayed a high
degree of temporal overlap. Anatomical reconstruction indicated that
the somatosensory input region includes, but may not be restricted to,
the caudomedial auditory association cortex. As was earlier reported
for this region, auditory frequency tuning curves were broad and
band-passed noise responses were larger than pure tone responses. No
somatosensory responses were observed in A1. These findings suggest
a potential neural substrate for multisensory integration at an early
stage of auditory cortical processing.
INTRODUCTION
The brain’s ability to combine inputs from different sensory
modalities yields an enriched description of objects as well as
converging evidence concerning their position, movement, and
identity. For such “multisensory integration” to occur, requires
that at some point in sensory processing, excitatory signals
arising from different sense modalities converge onto either
single neurons or interconnected ensembles of neurons. In the
first case, single neurons would be directly excitable through
each modality. In the second case, single neurons would be
excitable through one modality and might also be subject to
Address for reprint requests: C. E. Schroeder, Cognitive Neuroscience and
Schizophrenia Program, Nathan Kline Institute for Psychiatric Research, 140
Old Orangeburg Rd., Bldg. 37, Orangeburg, NY 10962 (E-mail: schrod
@nki.rfmh.org).
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more subtle modulatory influences (excitatory and/or inhibitory) from the other. Although neither type of convergence
guarantees occurrence of multisensory interactions (Stein and
Meredith 1993), they collectively provide the necessary anatomical substrates for such interactions. Definition of the brain
areas in which convergence occurs is therefore fundamental to
our understanding of the brain mechanisms of multisensory
processing and integration.
Prior studies in primates have demonstrated multisensory
convergence in parietal (e.g., Duhamel et al. 1998; Hyvarinen
and Shelepin 1979), temporal (e.g., Benevento et al. 1977;
Bruce et al. 1981; Leinonen et al. 1980), and frontal regions of
neocortex (e.g., Graziano et al. 1994; Rizzolatti et al. 1981). It
is noteworthy that these studies typically find both “multisensory” neurons with clear excitatory inputs from two or more
modalities (i.e., convergence at the neuronal level) and, in the
same cortical area, intermingled populations of apparently
“unimodal” neurons with different input sources (i.e., convergence at the areal/ensemble level).
The present study expands on a preliminary finding of a
somatosensory input to auditory association cortex. Our methods entail analysis of current source density (CSD) and multiunit action potential profiles sampled with linear array multielectrodes in awake monkeys. CSD analysis provides an
estimate of transmembrane current flow, which is the firstorder response to synaptic input. Analysis of concomitant
multiunit activity reveals the degree to which synaptic activity
generates a net change in local action potentials. Collection of
these measures with a linear array electrode enables us to
gauge the laminar activation sequence, which helps to differentiate feedforward from feedback and lateral input patterns
(Schroeder et al. 1995, 1998). While these methods do not
address convergence at the single neuron level, they provide
for an efficient, well-controlled evaluation of multisensory
convergence at the neuronal ensemble level.
METHODS
One rhesus and two cynomologus macaques (Maccaca mulatta and
M. fascicularis), weighing 5– 8 kg, were prepared for chronic awake
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0022-3077/01 $5.00 Copyright © 2001 The American Physiological Society
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SOMATOSENSORY INPUT TO AUDITORY CORTEX IN MACAQUES
recording used aseptic techniques, under general anesthesia (pentobarbital sodium, 25–35 mg/kg iv) (Schroeder et al. 1998). During
recording, animals were monitored continuously using electroencephalography (EEG) and video displays and were maintained in an
alert state but were not required to attend or discriminate stimuli in
any sensory modality. Laminar CSD and multiunit activity (MUA)
profiles were collected bilaterally from sites in A1 and the adjacent
regions posterior to A1, concentrating on caudomedial (CM) auditory
cortex. CSD profiles were calculated from field potential profiles
using a three-point formula for estimation of the second spatial
derivative of voltage (Freeman and Nicholson 1975; Nicholson and
Freeman 1975). MUA was obtained from the signal at each contact by
high-pass filtering the amplifier output at 500 Hz to isolate action
potential-frequency activity, full-wave rectifying the high-frequency
activity, and averaging the single sweep responses together. With the
rectification step, each averaged MUA tracing (see e.g., Fig. 1) is in
effect an action potential histogram; upward deflection represents
activity increase and downward deflection represents activity decrease
relative to the prestimulus baseline. See Schroeder et al. (1998) for
further details and illustration of these methods.
Figure 1 illustrates the positioning of the electrode array for laminar
profile analyses. For quantification, CSD profiles were full-wave
rectified, then averaged into a single waveform (AVREC; see Fig. 1),
and grand mean responses were computed across subjects.
Auditory stimuli were delivered at 65 dB (SPL) binaurally through
Sennheisser HD565 headphones coupled with 50-ml tubes placed
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against the external auditory canal (Javitt et al. 1996). A combination
of 100-␮s clicks and 100-ms pure tones and band-passed noise (5 ms
on/off ramps) was used to characterize best frequency and to optimize
stimulation at each recording site. For routine assessment of the best
frequency at each site, we analyzed responses to pure tones presented
at 2/s (Steinschneider et al. 1998). Specifically we measured the peak
of the MUA onset, in a window of 0 –50 ms poststimulus, at the
Lamina 3– 4 border. At each site, a first approximation of the tuning
curve was derived by taking this measurement from responses to 0.5,
1, 2, 4, 8, 16, 20, and 30 kHz. In some cases, the tuning estimate was
further refined as indicated by the first approximation, but the first
approximation was the only measure available for all recording sites.
Averaged responses to optimized stimuli were obtained at each
recording site. Co-located somatosensory responses were quantified
using electrical stimulation of peripheral nerves from the hand;
100-␮s square-wave (constant current) electrical pulses were delivered with gold cup EEG electrodes to the skin over the median nerve
in the forearm contralateral to the recording site (Peterson et al. 1995;
Schroeder et al. 1995, 1997) and constant 80-dB white noise masked
any co-incident auditory stimulation. It was established earlier that
repetitive electrical stimulation of the median nerve at the wrist
produces an averaged response in somatosensory cortex, extremely
similar to that produced by repetitive cutaneous stimulation of the
appropriate (radial) half of the glabrous hand surface. Specifically,
Schroeder et al. (1995) showed that in “median nerve territory in
primate Area 3b, the timing and distribution of action potentials and
FIG. 1. Laminar current source density (CSD) and concomitant multiunit activity (MUA) profiles (each an average of 100 trials)
sampled using a multielectrode with a linear array of recording contacts (150-␮m spacing) straddling auditory Area CM. Auditory
(left) and somatosensory (right) responses were elicited in this site by binaural 65 dB clicks and contralateral median nerve stimuli,
respectively. Downward CSD deflections (dark) signify net extracellular current sinks (inward transmembrane current); upward
deflections (stippled) indicate net extracellular current sources (outward current). MUA histograms are obtained by full-wave
rectification and averaging of the high-frequency activity at each electrode contact. The boxes circumscribe CSD configurations that
reflect the initial excitatory response at the depth of Lamina 4, and the subsequent excitation of the pyramidal cell ensembles in
Laminae 2/3. Scale bar (bottom right) ⫽ 1.4 mv/mm2 for CSD, 0.1 mv/mm2 for AVREC, and 1.6 ␮V for MUA.
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SCHROEDER, LINDSLEY, SPECHT, MARCOVICI, SMILEY, AND JAVITT
CSD components evoked by electrical stimulation of median nerve
and by stimulation of the volar surface of digit 1, were equivalent”
(see Schroeder et al. 1995, Fig. 1 vs. 3A). In the same recording site,
neither electrical stimulation of the ulnar nerve nor cutaneous stimulation of the volar surface of digit 5 produced a measurable response
(Schroeder et al. 1995, Figs. 2B and 3C). Thus median nerve electrical
stimulation clearly produces a specific “somatosensory” response. In
the present study, the definition of the median nerve-evoked response
as a somatosensory response is supported by the specificity of its
cortical distribution (see following text).
Recording sites were confirmed by histological analyses. Serial
sections were made and every third one was stained for Nissl substance, acetylcholine esterase (AchE) or parvalbumin (PV) to help
determine the borders between A1 and surrounding regions (Hackett
et al. 1998; Kosaki et al. 1997; Morel et al. 1993).
RESULTS
Areal convergence of somatosensory and auditory inputs, as
illustrated in Fig. 1, was found in 10/18 sites we examined that
were in auditory cortex, immediately posterior to A1. As
detailed in the following text, somato-auditory convergence
sites were concentrated in the caudomedial (CM) belt region of
auditory association cortex. The laminar profiles of co-represented auditory and somatosensory responses describe a characteristic activation sequence triggered by ascending synaptic
inputs in sensory cortex (Schroeder et al. 1995, 1998; Steinschneider et al. 1998): initial depolarization of input terminals
FIG. 2. Laminar CSD profiles (each an average of 100 trials) sampled from
an additional CM site, like that described in Fig. 1. Profiles are displayed on
an expanded scale to allow resolution of the laminar activation profile. All
stimulation and CSD conventions are the same as in Fig. 1.
FIG. 3. Top: AVREC CSD representations depicting somatosensory-auditory co-representation from single recording locations in each of the 3 monkeys in this study. Below this are across-subject grand mean AVRECs from
taken from the CM sites (10/18) that contained a somatosensory input from the
hand. Bottom: across-subject mean AVRECs showing clear auditory responses
and a lack of somatosensory responses in A1 (10 sites). Scale bars ⫽ 0.1
mV/mm2.
in and near Lamina 4, along with discharge of stellate cells,
producing a current sink over source configuration (lower
boxes) and associated action potentials, followed by excitation
of supra- and infragranular pyramidal cells. To allow better
visualization of the temporal pattern of synaptic activation in
Lamina 4 and lower Lamina 3, data from an additional somatosensory input site in auditory cortex are presented on an
expanded scale in Fig. 2. The excitatory CSD configuration in
supragranular pyramidal cells is typically source/sink (upper
boxes, Fig. 1), with associated action potentials displaced
below this to the base of Lamina 3. With the stimuli used here,
only the initial phase of excitation in the pyramidal cell ensemble is reflected in action potentials.
Under the present conditions, somatosensory and auditory
responses in CM begin at nearly the same time and have
similar amplitude at the first response peak; however, the
former tend to have larger amplitude during the later time
course of the response. This is shown by representative patterns of auditory and somatosensory response from single
penetration sites in each of the three monkeys (Fig. 3A) and the
grand mean data for the same conditions, across subjects, in
CM (Fig. 3B).
A1 penetrations, as distinguished by anatomical location
(see penetration 1, Fig. 4A), demonstrated no somatosensory
responsiveness (Fig. 3C). This fact supports the sensory specificity of the median nerve-evoked response (Schroeder et al.
1995). Sites displaying somato-auditory co-representation
were located in the caudal belt/parabelt regions. Reconstruction of three penetrations through this region is illustrated in
Fig. 4B. Two of these were in medial sites (3 and 4) and
showed clear somatosensory responsiveness, while the penetration through a more lateral site (2) showed none. All sites
SOMATOSENSORY INPUT TO AUDITORY CORTEX IN MACAQUES
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discussed in this report had robust auditory responses. The
overall distribution of auditory alone and somato-auditory convergence sites is represented in Fig. 4C. As illustrated there,
somato-auditory convergence sites appeared concentrated in
the CM but may extend posterior to CM into the adjacent
parabelt.
As reported earlier (Merzenich and Brugge 1973; Rauschecker et al. 1995, 1997; Recanzone et al. 2000a), frequency
tuning in posterior sites (Fig. 5, B and C) was broad relative to
that in A1 (Fig. 5A). This is apparent even with the approximation methods used in this study. With the same methods, the
sharpness of best frequency tuning in sites showing somatosensory input in the regions posterior to A1 (Fig. 5B) cannot be
distinguished from that in sites unresponsive to median nerve
stimulation (Fig. 5C). We would not rule out the possibility
that more precise testing in a larger sample would show such
a distinction.
DISCUSSION
The present study demonstrates areal convergence of somatosensory and auditory inputs within posterior auditory as-
FIG. 4. A: a parvalbumin (PV) immunolabled section showing an electrode
penetration (1) in the PV-rich zone that corresponds to A1. B: a section through
auditory association cortex posterior to A1 in the same hemisphere, lacking the
PV-rich zone corresponding to A1. Arrows mark the point at which each of the
3 visible electrode tracks (2– 4) sampled from auditory cortex. LS, lateral
sulcus. C: a depiction of the recording sites examined in this study. To make
this figure, the pattern of penetrations in each of the 6 brain hemispheres we
sampled was reconstructed with respect to the caudal border of A1, and these
were collapsed across hemispheres and subjects and registered onto the histological reconstruction of caudal superior temporal plane in one subject. The
sections were separated by 800 ␮m.
FIG. 5. Auditory frequency tuning curves for recording sites in A1 (A)
and for sites posterior to A1, including those exhibiting convergent somatosensory input (B) as well as those posterior sites without convergent
somatosensory input (C). Values represent the response to each stimulus
frequency as a percentage of the peak amplitude for the largest multiunit
response measured at the Lamina 3/4 border in each recording site. See text
for further details.
sociation cortex in the macaque monkey. The convergence
appeared concentrated in Area CM but may not be confined to
this area. Because CM represents an early stage of cortical
auditory processing, only one step removed from A1 (Kaas et
al. 1999; Rauschecker et al. 1997; Recanzone et al. 2000b;
Romanski et al. 1999), the somatosensory input is unexpected.
The only functional indications of somato-auditory conver-
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SCHROEDER, LINDSLEY, SPECHT, MARCOVICI, SMILEY, AND JAVITT
gence in this region are indirect and come from human experiments. Magnetoencephalographic recordings (Levanen et al.
1998) have localized vibration-induced activation within auditory cortex in congenitally deaf humans. Although it should be
emphasized that this result has not been shown in subjects with
normal hearing, event-related potential (ERP) studies in normal humans have observed short-latency somato-auditory integration effects having a time course and voltage topography
consistent with an ERP generator source in the superior temporal plane (Foxe et al. 2000).
Both the auditory and somatosensory activation profiles in
CM have a characteristic “feedforward” pattern, predicted by
the anatomy of feedforward projections (Rockland and Pandya
1979); excitation begins in Lamina 4 and spreads to the extragranular layers (Fig. 2). Although spatially overlapping neuronal populations in CM are clearly activated by each modality
(areal convergence), the proportion of local neurons that exhibit excitatory somato-auditory convergence relative to those
with unisensory excitatory input remains to be determined.
Even assuming that there is excitatory convergence in a high
proportion of single neurons, the strength and nature of any
resulting multisensory interactions is an open question, which
we are presently unable to resolve. We regard the actual
integration of somatosensory and auditory input within CM
neurons as a likely possibility, although alternatives are equally
interesting. Independent use of single neurons (or intermingled
populations of neurons) by separate sensory modalities, for
example, would represent a novel and intriguing use of cortical
architecture.
An earlier study observed somato-auditory convergence
within single units in area Tpt (Leinonen et al. 1980), but Tpt
is within the “parabelt” region of auditory cortex (Hackett et al.
1998), whereas our recordings were mainly in CM, which
corresponds to a part of the “belt” region of auditory cortex
(Hackett et al. 1998). Several studies have suggested that body
maps exist in the region caudolateral to the insula and SII/PV
cortices (Burton and Robinson 1981; Krubitzer et al. 1995;
Leinonen 1980; Robinson and Burton 1980). However, because none of these investigated somato-auditory convergence,
the degree of correspondence, if any, between the somatosensory inputs we describe and those defined earlier is not yet
clear.
In the present study, somatosensory stimulation was confined to the afferents from the hand, and thus we cannot
comment on the nature of the body map in CM. Krubitzer et al.
(1995) reported one or more partial body maps that abut the
SII/PV body maps in the fundus of the lateral sulcus and extend
out onto the superior temporal plane; that is, into a region that
very likely includes CM. This finding clearly predicts the
somato-auditory convergence we report here but does not tell
us whether CM contains a full body map or a representation
that is biased toward a particular surface(s), similar to the
“hand-” and “face-biases” found for somatic input to visual
areas MIP and VIP (Duhamel et al. 1998). This question is a
specific target of our ongoing studies.
The functional significance of somato-auditory convergence
in CM may be related to spatial localization in keeping with the
hypothesis that the caudal auditory cortices in general are
specialized for this function (Kaas 1999; Rauschecker et al.
1995; Romanski 2000). There does appear to be spatial correspondence between the auditory and somatosensory receptive
fields of Tpt neurons (Leinonen et al. 1980), but this has not
been investigated in CM. While there are only a few studies of
spatial receptive fields in auditory cortical neurons (Ahissar et
al. 1992; Benson et al. 1981; Recanzone et al. 2000), one of
these does suggest a special role for CM in sound localization
(Recanzone et al. 2000). A related possibility is that caudal
auditory regions are part of a network that combines vestibular
with other sensory inputs to compute the position of the head
in space and/or in relation to the other parts of the body
(Gulden and Grusser 1998). Somato-auditory convergence
would be extremely useful in such computations.
We thank Dr. P. Thier for helpful discussion on vestibular system projections and J. J. Foxe, T. McGinnis, E. Dias, and R. Feldman for technical and
conceptual assistance.
This work was supported in part by National Institute of Mental Health
Grants MH-61989 and MH-55620.
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