SUMMARY Spatial patterns of functional organization, resolved by microelectrode mapping, comprise a core principle of sensory cortices. In auditory cortex, however, recent two-photon Ca2+ imaging challenges this precept, as the traditional tonotopic arrangement appears weakly organized at the level of individual neurons. To resolve this fundamental ambiguity about the organization of auditory cortex, we developed multiscale optical Ca2+ imaging of unanesthetized GCaMP transgenic mice. Single-neuron activity monitored by two-photon imaging was precisely registered to large-scale cortical maps provided by transcranial wide field imaging. Neurons in the primary field responded well to tones, neighboring neurons were appreciably co-tuned, and preferred frequencies adhered tightly to a tonotopic axis. By contrast, nearby secondary-field neurons exhibited heterogeneous tuning. The multiscale imaging approach also readily localized vocalization regions and neurons. Altogether, these findings cohere electrode and two-photon perspectives, resolve new features of auditory cortex, and offer a promising approach generalizable to any cortical area.
1. The responses of neurons in the ventral cochlear nucleus (VCN) of decerebrate cats are described with regard to their regularity of discharge and latency. Regularity is measured by estimating the mean and standard deviation of interspike intervals as a function of time during responses to short tone bursts (25 ms). This method extends the usual interspike-interval analysis based on interval histograms by allowing the study of temporal changes in regularity during transient responses. The coefficient of variation (CV), equal to the ratio of standard deviation to mean interspike interval, is used as a measure of irregularity. Latency is measured as the mean and standard deviation of the latency of the first spike in response to short tone bursts, with 1.6-ms rise times. 2. The regularity and latency properties of the usual PST histogram response types are shown. Five major PST response type classes are used: chopper, primary-like, onset, onset-C, and unusual. The presence of a prepotential in a unit's action potentials is also noted; a prepotential implies that the unit is recorded from a bushy cell. 3. Units with chopper PST histograms give the most regular discharge. Three varieties of choppers are found. Chop-S units (regular choppers) have CVs less than 0.35 that are approximately constant during the response; chop-S units show no adaptation of instantaneous rate, as measured by the inverse of the mean interspike interval. Chop-T units have CVs greater than 0.35, show an increase in irregularity during the response and show substantial rate adaptation. Chop-U units have CVs greater than 0.35, show a decrease in irregularity during the response, and show a variety of rate adaptation behaviors, including negative adaptation (an increase in rate during a short-tone response). Irregular choppers (chop-T and chop-U units) rarely have CVs greater than 0.5. Choppers have the longest latencies of VCN units; all three groups have mean latencies at least 1 ms longer than the shortest auditory nerve (AN) fiber mean latencies. 4. Chopper units are recorded from stellate cells in VCN (35, 42). Our results for chopper units suggest a model for stellate cells in which a regularly firing action potential generator is driven by the summation of the AN inputs to the cell, where the summation is low-pass filtered by the membrane capacitance of the cell.(ABSTRACT TRUNCATED AT 400 WORDS)
This paper is concerned with the representation of the spectra of synthesized steady-state vowels in the temporal aspects of the discharges of auditory-nerve fibers. The results are based on a study of the responses of large numbers of single auditory-nerve fibers in anesthetized cats. By presenting the same set of stimuli to all the fibers encountered in each cat, we can directly estimate the population response to those stimuli. Period histograms of the responses of each unit to the vowels were constructed. The temporal response of a fiber to each harmonic component of the stimulus is taken to be the amplitude of the corresponding component in the Fourier transform of the unit's period histogram. At low sound levels, the temporal response to each stimulus component is maximal among units with CFs near the frequency of the component (i.e., near its place). Responses to formant components are larger than responses to other stimulus components. As sound level is increased, the responses to the formants, particularly the first formant, increase near their places and spread to adjacent regions, particularly toward higher CFs. Responses to nonformant components, exept for harmonics and intermodulation products of the formants (2F1,2F2,F1 + F2, etc), are suppressed; at the highest sound levels used (approximately 80 dB SPL), temporal responses occur almost exclusively at the first two or three formants and their harmonics and intermodulation products. We describe a simple calculation which combines rate, place, and temporal information to provide a good representation of the vowels' spectra, including a clear indication of at least the first two formant frequencies. This representation is stable with changes in sound level at least up to 80 dB SPL; its stability is in sharp contrast to the behavior of the representation of the vowels' spectra in terms of discharge rate which degenerates at stimulus levels within the conversational range.
1. Single-unit responses in the dorsal cochlear nucleus of unanesthetized, decerebrate cats have been divided into two categoreis. These have been differentiated on the basis of responses to best-frequency tones. Type IV units responded to best-frequency tones with excitation from threshold to about 20 or 30 dB above threshold; at higher levels, their response was inhibitory. In a few cases, the excitatory area near threshold was not seen and in a few others, the response became excitatory again at high levels. Type IV units could be divided into two groups based on the length of time that inhibition was maintained in response to long tones. Type IV units are not seen in anesthetized cats. 2. Type II/III units responded to best-frequency tones of all levels with excitation. Nonmonotonic rate versus level functions were seen in type II/III units, but they were of much less drastic character; the discharge rate of nonmonotonic type II/III units was still well above spontaneous rate for tones 50 dB above threshold. Type II/III units defined in this way were found to have, on the average, lower rates of spontaneous activity and higher thresholds than type IV units. 3. Type II/III units responded weakly to broad-band noise in comparison to auditory nerve fibers and many of them did not respond at all to noise. Type IV units, with best frequencies above 0.9 kHz, gave excitatory responses to noise. 4. The inhibitory response areas of type IV units could be divided into two areas: a central inhibitory area in the vicinity of best frequency where on- and off-discharges and afterdischarges were seen; and inhibitory side bands at higher and lower frequencies where simple inhibitory responses were seen. In four units, it was possible to show that the central inhibitory area was converted to an excitatory area after administration of an anesthetic dose of pentobarbital. 5. Most type II/III and type IV units could be excited or inhibited by stimuli in the contralateral ear. Broad-band noise was a more effective contralateral stimulus than tones at the ipsilateral best frequency. 6. On the basis of the properties of type II/III and type IV cells, it is suggested that type II/III responses are recorded from interneurons which provide a large share of the inhibitory imput to type IV cells.
Information processing by a sensory system is reflected in the changes in stimulus representation along its successive processing stages. We measured information content and stimulus-induced redundancy in the neural responses to a set of natural sounds in three successive stations of the auditory pathway-inferior colliculus (IC), auditory thalamus (MGB), and primary auditory cortex (A1). Information about stimulus identity was somewhat reduced in single A1 and MGB neurons relative to single IC neurons, when information is measured using spike counts, latency, or temporal spiking patterns. However, most of this difference was due to differences in firing rates. On the other hand, IC neurons were substantially more redundant than A1 and MGB neurons. IC redundancy was largely related to frequency selectivity. Redundancy reduction may be a generic organization principle of neural systems, allowing for easier readout of the identity of complex stimuli in A1 relative to IC.
A population study of cat auditory-nerve fibers was used to characterize the permanent deficits induced by exposure to 110-115 dB SPL, narrow-band noise. Fibers in the region of acoustic trauma (roughly 1-6 kHz) showed a loss of sensitivity at best frequency (BF) of about 50-60 dB and an increased tuning bandwidth. A correlation between weakened two-tone suppression and loss of sensitivity was found for fibers with BFs above 1 kHz. Single-fiber responses to the vowel "eh" were recorded at intensities ranging from near threshold to a maximum of about 110 dB SPL. In normal cochleas, the temporal response patterns show a capture phenomenon, in which the first two formant frequencies dominate the responses at high sound levels among fibers with BFs near the formant frequencies. After acoustic trauma, fibers in the region of threshold shift synchronized to a broad range of the vowel's harmonics and thus did not show capture by the second formant at any sound level used. The broadband nature of this response is consistent with the broadened tuning observed in the damaged fibers, but may also reflect a weakening of compressive nonlinearities responsible for synchrony capture in the normal cochlea.
This study describes the effects of broadband background noise on the average discharge rate to best-frequency (BF) tones of auditory nerve fibers in the cat. The effects of exposure to long-term continuous noise are compared to the effects of noise gated on and off simultaneously with test tones. Addition of background noise causes a shift of the dynamic portion of tone-evoked rate versus level functions to higher tone intensities. The shift occurs at a mean rate of 0.61 dB of shift for each 1-dB increment in noise level. The rate of shift is independent of best frequency and spontaneous discharge rate. The noise level at which the shift begins is frequency dependent and is consistent with the frequency-dependent bandwidths of auditory nerve fiber tuning curves. The adjustment of the dynamic range shows many similarities to two-tone suppression. Therefore, it is most likely that it is caused by suppression of the response to the BF test tone by energy present in the noise at surrounding frequencies. At high noise levels, the ability of auditory nerve fibers to respond to test tones is limited by the rate response to the noise. As noise level increases, the discharge rate it evokes approaches a fiber's saturation rate and ultimately eliminates the fiber's ability to respond to test tones. Low spontaneous rate fibers, which have been shown to have higher thresholds and wider dynamic range (17,29), are significantly more resistant to saturation by high noise levels. Exposure to broadband noise prior to onset of test tones produces an overall decrement in response rate. This phenomenon is similar to the effects of short-term adaptation (32) and seems to develop independently of the shift of dynamic range. At high noise levels, previous exposure to the noise produces a small dynamic range shift. This effect is similar to that produced by suppression but is smaller. The effect is occluded in continuous noise backgrounds by the adjustment of sensitivity produced by suppression.
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