Parallels Between Timing of Onset Responses of Single Neurons in Cat and of Evoked Magnetic Fields in Human Auditory Cortex

2000 ◽  
Vol 84 (5) ◽  
pp. 2426-2439 ◽  
Author(s):  
Silke Biermann ◽  
Peter Heil

Sound onsets constitute particularly salient transients and evoke strong responses from neurons of the auditory system, but in the past, such onset responses have often been analyzed with respect to steady-state features of sounds, like the sound pressure level. Recent electrophysiological studies of single neurons from the auditory cortex of anesthetized cats have revealed that the timing and strength of onset responses are shaped by dynamic stimulus properties at their very onsets. Here we demonstrate with magnetoencephalography that stimulus-response relationships very similar to those of the single neurons are observed in two onset components, N100m and P50m, of auditory evoked magnetic fields (AEFs) from the auditory cortex of awake humans. In response to tones shaped with cosine-squared rise functions, N100m and P50m peak latencies vary systematically with tone level and rise time but form a rather invariant function of the acceleration of the envelope at tone onset. Hence N100m and P50m peak latencies, as well as peak amplitudes, are determined by dynamic properties of the stimuli within the first few milliseconds, though not necessarily by acceleration. The changes of N100m and P50m peak latencies with rise time and level are incompatible with a fixed-amplitude threshold model. The direct comparison of the neuromagnetic and single-neuron data shows that, on average, the variance of the neuromagnetic data is larger by one to two orders of magnitude but that favorable measurements can yield variances as low as those derived from neurons with mediocre precision of response timing. The striking parallels between the response timing of single cortical neurons and of AEFs provides a stronger link between single neuron and population activity.

1988 ◽  
Vol 59 (5) ◽  
pp. 1524-1539 ◽  
Author(s):  
D. P. Phillips

1. The responses of cat auditory cortex neurons are largely dominated by transient stimulus events, including tone-pulse onset. In addition, these neurons often receive sensitive inhibitory inputs in tone frequency-intensity domains flanking the excitatory one centered at characteristic frequency (CF). These observations suggest that auditory cortex neurons might be sensitive to the spectral splatter that occurs at tone onset due to the tone-pulse envelope shape. 2. To investigate this hypothesis, single neurons in the primary auditory cortex of anesthetized cats were studied for the form of their spike-rate versus tone-level functions using CF tone pulses of different rise times. Stimuli were presented to the contralateral ear using a calibrated, sealed stimulus delivery system. 3. Some neurons with monotonic rate-level functions for conventional (5-10 ms) rise-time tones were relatively insensitive to variations in tone-pulse rise time. Other monotonic neurons showed rate-level functions that became increasingly bell shaped for shorter rise-time stimuli. All neurons with bell-shaped, nonmonotonic rate-level functions for conventional rise-time tones became increasingly nonmonotonic for shorter rise-time signals. In the same neurons, lengthening of tone rise times typically reduced the slope of the high-intensity, descending limb of the rate-level function, in some cases to zero. 4. This pattern of rise-time effects is consistent with previous evidence on the association between rate-level function shape and the presence of inhibitory tone response areas flanking the excitatory one at CF. The present data suggest that cortical neurons are sensitive to the gross shape of the short-term stimulus spectrum at tone onset, and that for many neurons, the nonmonotonic form of CF tone rate level functions may be configured as much by the rate of tone onset as by the plateau amplitude of a tone pulse.


2007 ◽  
Vol 97 (2) ◽  
pp. 1726-1737 ◽  
Author(s):  
M. L. Phan ◽  
G. H. Recanzone

One fundamental process of the auditory system is to process rapidly occurring acoustic stimuli, which are fundamental components of complex stimuli such as animal vocalizations and human speech. Although the auditory cortex is known to subserve the perception of acoustic temporal events, relatively little is currently understood about how single neurons respond to such stimuli. We recorded the responses of single neurons in the primary auditory cortex of alert monkeys performing an auditory task. The stimuli consisted of four tone pips with equal duration and interpip interval, with the first and last pip of the sequence being near the characteristic frequency of the neuron under study. We manipulated the rate of presentation, the frequency of the middle two tone pips, and the order by which they were presented. Our results indicate that single cortical neurons are ineffective at responding to the individual tone pips of the sequence for pip durations of <12 ms, but did begin to respond synchronously to each pip of the sequence at 18-ms durations. In addition, roughly 40% of the neurons tested were able to discriminate the order that the two middle tone pips were presented in at durations of ≥24 ms. These data place the primate primary auditory cortex at an early processing stage of temporal rate discrimination.


1984 ◽  
Vol 51 (5) ◽  
pp. 1028-1039 ◽  
Author(s):  
S. S. Orman ◽  
D. P. Phillips

In the auditory cortex of barbiturate-anesthetized cats, the posterior auditory field (area P) was identified by its tonotopic organization, and single neurons in that field were studied quantitatively with regard to their binaural interactions at their respective best frequencies, using calibrated, sealed stimulating systems. Almost 60% of the neurons studied displayed " summative " binaural interactions in that their responses to binaural, equally intense stimulation of the two ears were stronger than were their responses to monaural stimuli of the same intensity. For these neurons, latent periods were shorter for binaural stimuli than for monaural stimuli. Some field P neurons were sensitive to interaural intensity disparities and manifested that sensitivity in one of two forms. Cells that were excited by stimulation of one ear and inhibited by stimulation of the other typically displayed a sigmoidal relation of spike count to intensive disparity, with spike counts being larger when the disparity favored the contralateral ear. Cells that were unresponsive to monaural stimuli but responded securely to binaural stimuli usually displayed a peaked, nonmonotonic relation of spike count to interaural intensity disparity, with maximal responses being elicited by stimuli with zero or near-zero disparity. Some neurons of low best frequency were sensitive to variations in interaural phase delay. In all cases, this sensitivity was manifested as a cyclical relation of spike count to interaural delay, with the period of the cycle being that of the stimulating tone. The fact that the binaural interactions of field P neurons were similar to those of cells in the primary auditory cortex suggests that the previously described heightened spectral-amplitude selectivity of field P neurons has been achieved without cost to their sensitivity to a variety of parameters of binaural stimulation. The particular sensitivity of cortical neurons to variations in interaural disparities associated with midline or near-midline azimuths might constitute a neural mechanism for the behavioral finding that animals and humans show their greatest acuity in sound localization for stimulus locations in or near the midsagittal plane.


2020 ◽  
Author(s):  
Joshua D. Downer ◽  
Jessica R. Verhein ◽  
Brittany C. Rapone ◽  
Kevin N. O’Connor ◽  
Mitchell L. Sutter

ABSTRACTTextbook descriptions of primary sensory cortex (PSC) revolve around single neurons’ representation of low-dimensional sensory features, such as visual object orientation in V1, location of somatic touch in S1, and sound frequency in A1. Typically, studies of PSC measure neurons’ responses along few (1 or 2) stimulus and/or behavioral dimensions. However, real-world stimuli usually vary along many feature dimensions and behavioral demands change constantly. In order to illuminate how A1 supports flexible perception in rich acoustic environments, we recorded from A1 neurons while rhesus macaques performed a feature-selective attention task. We presented sounds that varied along spectral and temporal feature dimensions (carrier bandwidth and temporal envelope, respectively). Within a block, subjects attended to one feature of the sound in a selective change detection task. We find that single neurons tend to be high-dimensional, in that they exhibit substantial mixed selectivity for both sound features, as well as task context. Contrary to common findings in many previous experiments, attention does not enhance the single-neuron representation of attended features in our data. However, a population-level analysis reveals that ensembles of neurons exhibit enhanced encoding of attended sound features, and this population code tracks subjects’ performance. Importantly, surrogate neural populations with intact single-neuron tuning but shuffled higher-order correlations among neurons failed to yield attention-related effects observed in the intact data. These results suggest that an emergent population code not measurable at the single-neuron level might constitute the functional unit of sensory representation in PSC.SIGNIFICANCE STATEMENTThe ability to adapt to a dynamic sensory environment promotes a range of important natural behaviors. We recorded from single neurons in monkey primary auditory cortex while subjects attended to either the spectral or temporal features of complex sounds. Surprisingly, we find no average increase in responsiveness to, or encoding of, the attended feature across single neurons. However, when we pool the activity of the sampled neurons via targeted dimensionality reduction, we find enhanced population-level representation of the attended feature and suppression of the distractor feature. This dissociation of the effects of attention at the level of single neurons vs. the population highlights the synergistic nature of cortical sound encoding and enriches our understanding of sensory cortical function.


1992 ◽  
Vol 68 (5) ◽  
pp. 1487-1502 ◽  
Author(s):  
C. E. Schreiner ◽  
M. L. Sutter

1. The spatial distribution of the sharpness of tuning of single neurons along the dorsoventral extent of primary auditory cortex (AI) was studied. A sharpness of tuning gradient was initially obtained with multiple-unit recordings, and in combination with the cochleotopic organization, served as a frame of reference for the locations of single neurons. The frequency selectivity or "integrated excitatory bandwidth" of multiple units varied systematically along the dorsoventral extent of AI. The most sharply tuned unit clusters were found at the approximate center of the dorsoventral extent. A gradual broadening of the integrated excitatory bandwidth in both dorsal and ventral directions was consistently seen. 2. The multiple-unit measures of the bandwidth 10 (BW10) and 40 dB (BW40) above minimum threshold, pooled across several animals and expressed in octaves, were similar to those described within individual cases in cats. As in the individual animals, the bandwidth maps were V shaped with minima located at the approximate center of the dorsal-ventral extent of AI. The location of the minimum in the multiple-unit bandwidth map (i.e., the most sharply tuned area) was used as a reference point to pool single-neuron data across animals. 3. For single neurons, the dorsal half of the BW40 distribution showed a gradient paralleling that found for multiple units. For both single and multiple units, the average excitatory bandwidth increased at a rate of approximately 0.27 octaves/mm from the center of AI toward the dorsal fringe. Differing from the dorsal half of AI, the ventral half of AI showed no clear BW40 gradient for single units along its dorsoventral extent. At 40 dB above minimum threshold, most ventral neurons encountered were sharply tuned. By contrast, the multiple-unit BW40 showed a gradient similar to the dorsal half with 0.23 octaves/mm increasing from the center toward the ventral border of AI. 4. For single neurons, BW10 showed no clear systematic spatial distribution in AI. Neither the dorsal nor the ventral gradient was significantly different from zero slope, although the dorsal half showed a trend toward increasing BW10s. Contrasting single neurons, both dorsal and ventral halves of AI showed BW10 slopes for multiple units confirming a V-shaped map of the integrated excitatory bandwidth within the dorsoventral extent of AI. 5. On the basis of the distribution of the integrated (multiple-unit) excitatory bandwidth, AI was parceled into three regions: the dorsal gradient, the ventral gradient, and the central, narrowly tuned area.(ABSTRACT TRUNCATED AT 400 WORDS)


1995 ◽  
Vol 73 (2) ◽  
pp. 674-686 ◽  
Author(s):  
D. P. Phillips ◽  
M. N. Semple ◽  
L. M. Kitzes

1. The posterior field (field P) of the cat's auditory cortex contains a higher proportion of neurons whose response/level functions for characteristic frequency (CF) tones are nonmonotonic than does the primary field (AI). The general purpose of the present study is to assess whether the response/level functions of field P neurons are generated by the same mechanisms as those of cells in AI. All of the data came from single neurons in the cortices of barbiturate-anesthetized cats, to which we presented tonal stimuli through sealed, calibrated stimulating systems. 2. We obtained quantitative data from 123 neurons, of which 108 were located in field P. Of the 108 field P cells, 70% had nonmonotonic response/level functions for 5-ms rise time tones of CF. For cells of any given CF, both CF thresholds and best SPLs (i.e., SPLs associated with maximal responses) varied widely. A correlation analysis revealed that a linear relation between best SPL and CF threshold accounted for 73% of the data variance in the association between those response variables. An analysis of data from 83 nonmonotonic cells in AI revealed a similar relation. 3. Field P neurons whose response/level functions were non-monotonic for 5-ms rise time CF tones became even more narrowly tuned to SPL when the rise time of the tone bursts was reduced to 1 ms. Lengthening the rise time to 20 ms reduced or eliminated the SPL tuning in almost all of these neurons. The general form of monotonic tone response/level functions was commonly unaffected by variation in signal rise time. In a few instances, cells with monotonic response/level functions for 5- and 20-ms rise time tones developed nonmonotonic functions for 1-ms rise time tones. 4. Field P neurons with nonmonotonic response/level functions for CF tones usually failed to respond to wideband noise pulses, or, less commonly, responded to noise only at low SPLs. In contrast, field P cells with a monotonic response to CF tones usually responded monotonically to noise. 5. The minimal mean first-spike latencies of field P neurons were generally longer than those of AI cells studied under similar conditions. The precision of first-spike timing, measured using the SD of the mean first-spike latency, was commonly poorer than that of AI cells. 6. The properties of field P cells followed the same rules as those seen in AI.(ABSTRACT TRUNCATED AT 400 WORDS)


2020 ◽  
Author(s):  
Francisca Machado ◽  
Nuno Sousa ◽  
Patricia Monteiro ◽  
Luis Jacinto

AbstractThe demand for affordable tools for recording extracellular activity and successfully isolating single units from different brain preparations has pushed researchers and companies to invest in developing and fabricating new recording devices. However, depending on the brain region of interest, experimental question or type of preparations, different devices are required thus adding substantial financial burden to laboratories. We have developed a simple and affordable tetrode-based device that allows interchangeable extracellular recordings of neural activity between in vivo and ex vivo preparations and can be easily implemented in all wet-bench laboratories. Spontaneous activity from several putative single neurons could be easily recorded and isolated by lowering the device into ex vivo cerebellum brain slices. The same device was also used in vivo, lowered into primary auditory cortex of adult anesthetized transgenic mice expressing channelrhodopsin in cortical neurons. Acoustic stimulation of the contralateral ear or direct laser optogenetic stimulation successfully evoked cortical activity at the recording site. Several isolated putative single neurons presented time-locked activity response to the different stimuli. In summary, we developed an affordable, versatile and modular device to facilitate tetrode extracellular recordings interchangeably between in vivo anaesthetized animals and ex vivo brain slice recordings.HighlightsDeveloped a versatile and modular device to facilitate tetrode acute brain recordings interchangeably between in vivo and ex vivo preparations.Conducted ex vivo extracellular recordings in acute cerebellar slices.Conducted in vivo extracellular recordings in auditory cortex of anaesthetized mice.Recorded and isolated multiple single units in both acute slices and anaesthetized mice recordings using the same device.Device can be easily extended to accommodate optic fiber and cannula.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Jermyn Z. See ◽  
Natsumi Y. Homma ◽  
Craig A. Atencio ◽  
Vikaas S. Sohal ◽  
Christoph E. Schreiner

AbstractNeuronal activity in auditory cortex is often highly synchronous between neighboring neurons. Such coordinated activity is thought to be crucial for information processing. We determined the functional properties of coordinated neuronal ensembles (cNEs) within primary auditory cortical (AI) columns relative to the contributing neurons. Nearly half of AI cNEs showed robust spectro-temporal receptive fields whereas the remaining cNEs showed little or no acoustic feature selectivity. cNEs can therefore capture either specific, time-locked information of spectro-temporal stimulus features or reflect stimulus-unspecific, less-time specific processing aspects. By contrast, we show that individual neurons can represent both of those aspects through membership in multiple cNEs with either high or absent feature selectivity. These associations produce functionally heterogeneous spikes identifiable by instantaneous association with different cNEs. This demonstrates that single neuron spike trains can sequentially convey multiple aspects that contribute to cortical processing, including stimulus-specific and unspecific information.


1995 ◽  
Vol 73 (5) ◽  
pp. 1876-1891 ◽  
Author(s):  
M. B. Calford ◽  
M. N. Semple

1. Several studies of auditory cortex have examined the competitive inhibition that can occur when appropriate sounds are presented to each ear. However, most cortical neurons also show both excitation and inhibition in response to presentation of stimuli at one ear alone. The extent of such inhibition has not been described. Forward masking, in which a variable masking stimulus was followed by a fixed probe stimulus (within the excitatory response area), was used to examine the extent of monaural inhibition for neurons in primary auditory cortex of anesthetized cats (barbiturate or barbiturate-ketamine). Both the masking and probe stimuli were 50-ms tone pips presented to the contralateral ear. Most cortical neurons showed significant forward masking at delays beyond which masking effects in the auditory nerve are relatively small compared with those seen in cortical neurons. Analysis was primarily concerned with such components. Standard rate-level functions were also obtained and were examined for nonmonotonicity, an indication of level-dependent monaural inhibition. 2. Consistent with previous reports, a wide range of frequency tuning properties (excitatory response area shapes) was found in cortical neurons. This was matched by a wide range of forward-masking-derived inhibitory response areas. At the most basic level of analysis, these were classified according to the presence of lateral inhibition, i.e., where a probe tone at a neuron's characteristic frequency was masked by tones outside the limits of the excitatory response area. Lateral inhibition was a property of 38% of the sampled neurons. Such neurons represented 77% of those with nonmonotonic rate-level functions, indicating a strong correlation between the two indexes of monaural inhibition; however, the shapes of forward masking inhibitory response areas did not usually correspond with those required to account for the "tuning" of a neuron. In addition, it was found that level-dependent inhibition was not added to by forward masking inhibition. 3. Analysis of the discharges to individual stimulus pair presentations, under conditions of partial masking, revealed that discharges to the probe occurred independently of discharges to the preceding masker. This indicates that even when the masker is within a neuron's excitatory response area, forward masking is not a postdischarge habituation phenomenon. However, for most neurons the degree of masking summed over multiple stimulus presentations appears determined by the same stimulus parameters that determine the probability of response to the masker.(ABSTRACT TRUNCATED AT 400 WORDS)


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