Response selectivity for species-specific calls in the inferior colliculus of Mexican free-tailed bats is generated by inhibition

Here we show that inhibition shapes diverse responses to species-specific calls in the inferior colliculus (IC) of Mexican free-tailed bats. We presented 10 calls to each neuron of which 8 were social communication and 2 were echolocation calls. We also measured excitatory response regions: the range of tone burst frequencies that evoked discharges at a fixed intensity. The calls evoked highly selective responses in that IC neurons responded to some calls but not others even though those calls swept through their excitatory response regions. By convolving activity in the response regions with the spectrogram of each call, we evaluated whether responses to tone bursts could predict discharge patterns evoked by species-specific calls. The convolutions often predicted responses to calls that evoked no responses and thus were inaccurate. Blocking inhibition at the IC reduced or eliminated selectivity and greatly improved the predictive accuracy of the convolutions. By comparing the responses evoked by two calls with similar spectra, we show that each call evoked a unique spatiotemporal pattern of activity distributed across and within isofrequency contours and that the disparity in the population response was greatly reduced by blocking inhibition. Thus the inhibition evoked by each call can shape a unique pattern of activity in the IC population and that pattern may be important for both the identification of a particular call and for discriminating it from other calls and other signals.     

Differing roles of inhibition in hierarchical processing of species-specific calls in auditory brainstem nuclei

Here we report on response properties and the roles of inhibition in three brain stem nuclei of Mexican-free tailed bats: the inferior colliculus (IC), the dorsal nucleus of the lateral lemniscus (DNLL) and the intermediate nucleus of the lateral lemniscus (INLL). In each nucleus, we documented the response properties evoked by both tonal and species-specific signals and evaluated the same features when inhibition was blocked. There are three main findings. First, DNLL cells have little or no surround inhibition and are unselective for communication calls, in that they responded to approximately 97% of the calls that were presented. Second, most INLL neurons are characterized by wide tuning curves and are unselective for species-specific calls. The third finding is that the IC population is strikingly different from the neuronal populations in the INLL and DNLL. Where DNLL and INLL neurons are unselective and respond to most or all of the calls in the suite we presented, most IC cells are selective for calls and, on average, responded to approximately 50% of the calls we presented. Additionally, the selectivity for calls in the majority of IC cells, as well as their tuning and other response properties, are strongly shaped by inhibitory innervation. Thus we show that inhibition plays only limited roles in the DNLL and INLL but dominates in the IC, where the various patterns of inhibition sculpt a wide variety of emergent response properties from the backdrop of more expansive and far less specific excitatory innervation.     

Thalamocortical transformation of responses to complex auditory stimuli

Summary In unanesthetized guinea pigs, thalamic (CGM), and cortical (auditory I) neurons were recorded simultaneously. Nine of 69 neuron pairs showed a positive cross-correlation of their spontaneous activities, with increased discharge probability of the cortical neuron beginning 2–5 ms after the discharge of the CGM-neuron. The individual neurons of such pairs had an identical CF and the same spectral responsiveness.The responses of cortical neurons to pure tones were much more phasic than those of the corresponding CGM-neurons. Thalamic neurons could be driven up to much higher AM- and FM-modulation frequencies (100 Hz) than cortical neurons, which usually ceased to follow AM-frequencies above 20 Hz. Stronger or weaker suppression of tonic response components in cortical and thalamic neurons and the lower AM-range of cortical neurons is related to stronger or weaker intracortical and intrathalamic inhibition respectively. Response characteristics to FM-stimuli are similar to those of AM-stimuli.All CGM and cortical neurons responded to a variety of natural calls of the same or of other species. Responses of CGM-cells represented more components of a call than cortical cells even if the two cells were synaptically connected. In cortical cells, repetitive elements of a call were not represented if the repetition rate was too high. High modulation frequencies within a call, such as those of the fundamental frequency, could still be separated in the response of some CGM-neurons, but never in those of cortical neurons. Both CGM and cortical cells responded essentially to transients (amplitude or frequency modulations) within a call, if spectral components of such elements were within the spectral sensitivity of the cell. Spectral components outside the spectral sensitivity range could result in suppression of spontaneous discharge rate. Responses of cortical and CGM-cells, and thus the representation of call elements by neuronal responses, varied with the intensity of a call. It is suggested that, at higher levels of the auditory system, essential information about the temporal features of complex sounds may be represented by neural responses to transients in various spectral regions.This work was partially supported by the Deutsche Forschungsgemeinschaft through the Sonderforschungsbereich 33     

Basolateral amygdala responds robustly to social calls: spiking characteristics of single unit activity

Vocalizations emitted within a social context can trigger call-specific changes in the emotional and physiological/autonomic state of the receiver. The amygdala is implicated in mediating these changes, but its role in call perception remains relatively unexplored. We examined call and pitch selectivity of single neurons within the basolateral amygdala (BLA) by recording spiking activity in response to 5 pitch variants of each of 14 species-specific calls presented to awake, head-restrained mustached bats, Pteronotus parnellii. A response-wise analysis across neurons revealed seven types of temporal response patterns based on the timing and duration of spiking. Roughly half of the responses to different call types were significantly affected by changes in call pitch. A neuron-wise analysis revealed that ～ 12% (8/69) of the neurons preferred the same pitch across all call types. Ninety-three percent (93/100) of neurons were excited by at least one call type and 76% exhibited either complete or transient suppression to one or more call types. The majority of neurons preferred fewer than half of the 14 different simple-syllabic calls. A call-wise analysis of spiking activity revealed that call types signaling either threat or fear most consistently evoked increases in the spike rate. In contrast, calls emitted during appeasement tended to evoke spike suppression. Our data suggest that BLA neurons participate in the processing of multiple call types and exhibit a rich variety of temporal response patterns that are neither neuron nor call specific.     

Whole cell recordings of intrinsic properties and sound-evoked responses from the inferior colliculus

Response features of inferior colliculus (IC) neurons to both current injections and tone bursts were studied with in vivo whole cell recordings in awake Mexican free-tailed bats. Of 160 cells recorded, 95% displayed one of three general types of discharge patterns in response to the injection of positive current: 1) sustained discharges; 2) adapting discharges; and 3) onset-bursting discharges. Sustained neurons were the most common type (N=78), followed by onset-bursting (N=57). The least common type was adapting (N=17). In 90 neurons the profiles of synaptic and discharge activity evoked by tones of different frequencies at 50 dB SPL were recorded. Three major tone-evoked response profiles were obtained; 1) neurons dominated by excitation (N=32) in which tones evoked excitatory post-synaptic potentials (EPSPs) or EPSPs with discharges over a range of frequencies with little or no evidence of inhibitory post-synaptic potentials (IPSPs) evoked by frequencies that flanked the excitation; 2) neurons that had an excitatory frequency region in which discharges were evoked that was flanked by frequencies that evoked predominantly IPSPs (N=26); 3) neurons in which all frequencies evoked IPSPs with little or no depolarizations (N=32). The question we asked is whether IC cells that express a particular profile of PSPs and discharges to acoustic stimulation also have the same current-evoked response profile. We show that, with one exception, the intrinsic features of an IC neuron are not correlated with the pattern of its synaptic innervation; the two features are unrelated in the majority of IC cells. The exception is a subtype of inhibitory dominated cell where most frequencies evoked IPSPs to both the onset and to the offset of the tone bursts. In those cells injected current steps always evoked an onset-bursting response.     

Responses to social vocalizations in the inferior colliculus of the mustached bat are influenced by secondary tuning curves

Neurons in the inferior colliculus (IC) of the mustached bat integrate input from multiple frequency bands in a complex fashion. These neurons are important for encoding the bat's echolocation and social vocalizations. The purpose of this study was to quantify the contribution of complex frequency interactions on the responses of IC neurons to social vocalizations. Neural responses to single tones, two-tone pairs, and social vocalizations were recorded in the IC of the mustached bat. Three types of data driven stimulus-response models were designed for each neuron from single tone and tone pair stimuli to predict the responses of individual neurons to social vocalizations. The first model was generated only using the neuron's primary frequency tuning curve, whereas the second model incorporated the entire hearing range of the animal. The extended model often predicted responses to many social vocalizations more accurately for multiply tuned neurons. One class of multiply tuned neuron that likely encodes echolocation information also responded to many of the social vocalizations, suggesting that some neurons in the mustached bat IC have dual functions. The third model included two-tone frequency tunings of the neurons. The responses to vocalizations were better predicted by the two-tone models when the neuron had inhibitory frequency tuning curves that were not near the neuron's primary tuning curve. Our results suggest that complex frequency interactions in the IC determine neural responses to social vocalizations and some neurons in IC have dual functions that encode both echolocation and social vocalization signals.     

Representation of species-specific vocalizations in the inferior colliculus of the guinea pig

The responses of individual neurons to 4 typical guinea pig vocalization calls (purr, chutter, chirp, and whistle) were recorded in the inferior colliculus (IC) of anesthetized guinea pigs. All calls elicited a response in about 80% of units. Unit selectivity for individual calls was low, given that a majority of neurons (55% of 124 units) responded to all vocalizations and only a small portion of neurons (3%) responded to only one call or did not respond to any of the calls (3%). In 15% of units, the response to one call was > or =25% stronger than the response to any other sound (tone, noise, and other calls); these neurons were selective for chirp or whistle, and no unit preferred chutter or purr. Neuronal activity provided information about the spectrotemporal patterns of the calls. Peristimulus time histograms (PSTHs) reflected the energy of the near-characteristic frequency band, and the population PSTH reliably matched the sound envelope for calls characterized by one or more short impulses (chirp, purr, and chutter) but did not exactly fit the envelope for whistle--a slow-modulated and relatively long call. Calculations based on firing rates indicated the approximate positions of the main spectral peaks but did not always reflect their relative magnitude. The time-reversed version of whistle elicited on average a weaker response than did the natural whistle (by 24%), but there were neurons with a significantly stronger response to the natural ("forward-selective," 30%) as well as to the time-reversed whistle ("reverse-selective," 15%). This study does not prove the existence of units selectively responding to animal calls, but it provides evidence for the encoding of the spectrotemporal acoustic patterns of vocalizations by IC units.     

Representation of spectral and temporal envelope of twitter vocalizations in common marmoset primary auditory cortex

Cortical sensitivity in representations of behaviorally relevant complex input signals was examined in recordings from primary auditory cortical neurons (AI) in adult, barbiturate-anesthetized common marmoset monkeys (Callithrix jacchus). We studied the robustness of distributed responses to natural and degraded forms of twitter calls, social contact vocalizations comprising several quasi-periodic phrases of frequency and AM. We recorded neuronal responses to a monkey's own twitter call (MOC), degraded forms of their twitter call, and sinusoidal amplitude modulated (SAM) tones with modulation rates similar to those of twitter calls. In spectral envelope degradation, calls with narrowband channels of varying bandwidths had the same temporal envelope as a natural call. However, the carrier phase was randomized within each narrowband channel. In temporal envelope degradation, the temporal envelope within narrowband channels was filtered while the carrier frequencies and phases remained unchanged. In a third form of degradation, noise was added to the natural calls. Spatiotemporal discharge patterns in AI both within and across frequency bands encoded spectrotemporal acoustic features in the call although the encoded response is an abstract version of the call. The average temporal response pattern in AI, however, was significantly correlated with the average temporal envelope for each phrase of a call. Response entrainment to MOC was significantly correlated with entrainment to SAM stimuli at comparable modulation frequencies. Sensitivity of the response patterns to MOC was substantially greater for temporal envelope than for spectral envelope degradations. The distributed responses in AI were robust to additive continuous noise at signal-to-noise ratios > or =10 dB. Neurophysiological data reflecting response sensitivity in AI to these forms of degradation closely parallel human psychophysical results on the intelligibility of degraded speech in quiet and noisy conditions.     

Serotonin effects on frequency tuning of inferior colliculus neurons

We investigated the modulatory effects of serotonin on the tuning of 114 neurons in the central nucleus of the inferior colliculus (ICc) of Mexican free-tailed bats and how serotonin-induced changes in tuning influenced responses to complex signals. We obtained a "response area" for each neuron, defined as the frequency range that evoked discharges and the spike counts evoked by those frequencies at a constant intensity. We then iontophoretically applied serotonin and compared response areas obtained before and during the application of serotonin. In 58 cells, we also assessed how serotonin-induced changes in response areas correlated with changes in the responses to brief frequency-modulated (FM) sweeps whose structure simulated natural echolocation calls. Serotonin profoundly changed tone-evoked spike counts in 60% of the neurons (68/114). In most neurons, serotonin exerted a gain control, facilitating or depressing the responses to all frequencies in their response areas. In many cells, serotonergic effects on tones were reflected in the responses to FM signals. The most interesting effects were in those cells in which serotonin selectively changed the responsiveness to only some frequencies in the neuron's response area and had little or no effect on other frequencies. This caused predictable changes in responses to the more complex FM sweeps whose spectral components passed through the neurons' response areas. Our results suggest that serotonin, whose release varies with behavioral state, functionally reconfigures the circuitry of the IC and may modulate the perception of acoustic signals under different behavioral states.     

Auditory responsive cortex in the squirrel monkey: neural responses to amplitude-modulated sounds

The neural response to amplitude-modulated sinus sounds (AM sound) was investigated in the auditory cortex and insula of the awake squirrel monkey. It was found that 78.1% of all acoustically driven neurons encoded the envelope of the AM sound; the remaining 21.9% displayed simple On, On/Off or Off responses at the beginning or the end of the stimulus sound. Those neurons with AM coding were able to encode the AM sound frequency in two different ways: (1) the spikes followed the amplitude modulation envelopes in a phaselocked manner; (2) the spike rate changed significantly with changing modulation frequencies. As reported in other species, the modulation transfer functions for rate showed higher modulation frequencies than the phaselocked response. Both AM codings exhibited a filter characteristic for AM sound. Whereas 46.6% of all neurons had the same filter characteristic for both the spike discharge and the phase-locked response, the remaining neurons displayed combinations of different filter types. The discharge pattern of a neuron to simple tone or noise bursts suggests the behaviour of this neuron when AM sound is used as the stimulus. Neurons with strong onset responses to tone/noise bursts tended to have higher phase-locked AM responses than neurons with weak onset responses. The spike rate maxima for AM sound showed no relation to the tone/noise burst discharge patterns. Varying modulation depth was encoded by the neuron's ability to follow the envelope cycles and not by the non-phase-locked spike rate frequency. The organization of the squirrel monkey's auditory cortex has previously been established by an anatomical study. We have added two new fields using physiological parameters. All fields investigated showed a clear functional separation for time-critical information processing. The best temporal resolution was shown by the primary auditory field (AI), the first-temporal field (T1) and the parainsular au ditory field (Pi). The neural data in these fields and the amplitude modulation frequency range of squirrel monkey calls suggest a similar correlation between vocalization and perception as in human psychophysical data for speech and hearing sensation. The anterior fields in particular failed to follow the AM envelopes. For the first time in a primate, the insula was tested with different sound parameters ranging from simple tone bursts to AM sound. It is suggested that this cortical region plays a role in time-critical aspects of acoustic information processing. The observed best frequencies covered the same spectrum as AI. As in the auditory fields, most neurons in the insula encoded AM sound with different filter types. The high proportion of neurons unable to encode AM sound (40.6%) and the low mean best modulation frequency (9.9 Hz) do not support a prominent role of the insula in temporal information processing.     

Effects of auditory stimulus context on the representation of frequency in the gerbil inferior colliculus

Prior studies of dynamic conditioning have focused on modulation of binaural localization cues, revealing that the responses of inferior colliculus (IC) neurons to particular values of interaural phase and level disparities depend critically on the context in which they occur. Here we show that monaural frequency transitions, which do not simulate azimuthal motion, also condition the responses of IC neurons. We characterized single-unit responses to two frequency transition stimuli: a glide stimulus comprising two tones linked by a linear frequency sweep (origin-sweep-target) and a step stimulus consisting of one tone followed immediately by another (origin-target). Using sets of glide and step stimuli converging on a common target, we constructed conditioned response functions (RFs) depicting the variability in the response to an identical stimulus as a function of the preceding origin frequency. For nearly all cells, the response to the target depended on the origin frequency, even for origins outside the excitatory frequency response area of the cell. Results from conditioned RFs based on long (2-4 s) and short (200 ms) duration step stimuli indicate that conditioning effects can be induced in the absence of the dynamic sweep, and by stimuli of relatively short duration. Because IC neurons are tuned to frequency, changes in the origin frequency often change the "effective" stimulus duty cycle. In many cases, the enhancement of the target response appeared related to the decrease in the "effective" stimulus duty cycle rather than to the prior presentation of a particular origin frequency. Although this implies that nonselective adaptive mechanisms are responsible for conditioned responses, slightly more than half of IC neurons in each paradigm responded significantly differently to targets following origins that elicited statistically indistinguishable responses. The prevailing influence of stimulus context when discharge history is controlled demonstrates that not all the mechanisms governing conditioning depend on the discharge history of the recorded neuron. Selective adaptation among the neuron's variously tuned afferents may help engender stimulus-specific conditioning. The demonstration that conditioning effects reflect sensitivity to spectral as well as spatial stimulus contrast has broad implications for the processing of a wide range of dynamic acoustic signals and sound sequences.     

Responses of neurons in the rat's ventral nucleus of the lateral lemniscus to amplitude-modulated tones

Recordings were made from single neurons in the rat's ventral nucleus of the lateral lemniscus (VNLL) to determine responses to amplitude-modulated (AM) tones. The neurons were first characterized on the basis of their response to tone bursts presented to the contralateral ear and a distinction was made between those with transient onset responses and those with sustained responses. Sinusoidal AM tones were then presented to the contralateral ear with a carrier that matched the neuron's characteristic frequency (CF). Modulation transfer functions were generated on the basis of firing rate (MTF(FR)) and vector strength (MTF(VS)). Ninety-two percent of onset neurons that responded continuously to AM tones had band-pass MTF(FR)s with best modulation frequencies from 10 to 300 Hz. Fifty-four percent of sustained neurons had band-pass MTF(FR)s with best modulation frequencies from 10 to 500 Hz; other neurons had band-suppressed, all-pass, low-pass, or high-pass functions. Most neurons showed either band-pass or low-pass MTF(VS). Responses were well synchronized to the modulation cycle with maximum vector strengths ranging from 0.37 to 0.98 for sustained neurons and 0.78 to 0.99 for onset neurons. The upper frequency limit for response synchrony was higher than that reported for inferior colliculus, but lower than that seen in more peripheral structures. Results suggest that VNLL neurons, especially those with onset responses to tone bursts, are sensitive to temporal features of sounds and narrowly tuned to different modulation rates. However, there was no evidence of a topographic relation between dorsoventral position along the length of VNLL and best modulation frequency as determined by either firing rate or vector strength.     

Temporal measures and neural strategies for detection of tones in noise based on responses in anteroventral cochlear nucleus

To examine possible neural strategies for the detection of tones in broadband noise, single-neuron extracellular recordings were obtained from the anteroventral cochlear nucleus (AVCN) in anesthetized gerbils. Detection thresholds determined by average discharge rate and several temporal metrics were compared with previously reported psychophysical detection thresholds in cats (Costalupes 1985). Because of their limited dynamic range, the average discharge rates of single neurons failed to predict psychophysical detection thresholds for relatively high-level noise at all measured characteristic frequencies (CFs). However, temporal responses changed significantly when a tone was added to a noise, even for neurons with flat masked rate-level functions. Three specific temporal analyses were applied to neural responses to tones in noise. First, temporal reliability, a measure of discharge time consistency across stimulus repetitions, decreased with increasing tone level for most AVCN neurons at all measured CFs. Second, synchronization to the tone frequency, a measure of phase-locking to the tone, increased with tone level for low-CF neurons. Third, rapid fluctuations in the poststimulus time histograms (PSTHs) decreased with tone level for a number of neurons at all CFs. For each of the three temporal measures, some neurons had detection thresholds at or below psychophysical thresholds. A physiological model of a higher-stage auditory neuron that received simple excitatory and inhibitory inputs from AVCN neurons was able to extract the PSTH fluctuation information in a form of decreased rate with tone level.     

Physiological response properties of neurons in the superior paraolivary nucleus of the rat

The superior paraolivary nucleus (SPON) is a prominent nucleus of the superior olivary complex. In rats, this nucleus is composed of a morphologically homogeneous population of GABAergic neurons that receive excitatory input from the contralateral cochlear nucleus and inhibitory input from the ipsilateral medial nucleus of the trapezoid body. SPON neurons provide a dense projection to the ipsilateral inferior colliculus and are thereby capable of exerting profound modulatory influence on collicular neurons. Despite recent interest in the structural and connectional features of SPON, little is presently known concerning the physiological response properties of this cell group or its functional role in auditory processing. We utilized extracellular, in vivo recording methods to study responses of SPON neurons to broad band noise, pure tone, and amplitude-modulated pure tone stimuli. Localization of recording sites within the SPON provides evidence for a medial (high frequency) to lateral (low frequency) tonotopic representation of frequencies within the nucleus. Best frequencies of SPON neurons spanned the audible range of the rat and receptive fields were narrow with V-shaped regions near threshold. Nearly all SPON neurons responded at the offset of broad band noise and pure tone stimuli. The vast majority of SPON neurons displayed very low rates of spontaneous activity and only responded to stimuli presented to the contralateral ear, although a small population showed binaural facilitation. Most SPON neurons also generated spike activity that was synchronized to sinusoidally amplitude-modulated tones. Taken together, these data suggest that SPON neurons may serve to encode temporal features of complex sounds, such as those contained in species-specific vocalizations.     

Neural representations of sinusoidal amplitude and frequency modulations in the primary auditory cortex of awake primates

We investigated neural coding of sinusoidally modulated tones (sAM and sFM) in the primary auditory cortex (A1) of awake marmoset monkeys, demonstrating that there are systematic cortical representations of embedded temporal features that are based on both average discharge rate and stimulus-synchronized discharge patterns. The rate-representation appears to be coded alongside the stimulus-synchronized discharges, such that the auditory cortex has access to both rate and temporal representations of the stimulus at high and low frequencies, respectively. Furthermore, we showed that individual auditory cortical neurons, as well as populations of neurons, have common features in their responses to both sAM and sFM stimuli. These results may explain the similarities in the perception of sAM and sFM stimuli as well as the different perceptual qualities effected by different modulation frequencies. The main findings include the following. 1) Responses of cortical neurons to sAM and sFM stimuli in awake marmosets were generally much stronger than responses to unmodulated tones. Some neurons responded to sAM or sFM stimuli but not to pure tones. 2) The discharge rate-based modulation transfer function typically had a band-pass shape and was centered at a preferred modulation frequency (rBMF). Population-averaged mean firing rate peaked at 16- to 32-Hz modulation frequency, indicating that the A1 was maximally excited by this frequency range of temporal modulations. 3) Only approximately 60% of recorded units showed statistically significant discharge synchrony to the modulation waveform of sAM or sFM stimuli. The discharge synchrony-based best modulation frequency (tBMF) was typically lower than the rBMF measured from the same neuron. The distribution of rBMF over the population of neurons was approximately one octave higher than the distribution of tBMF. 4) There was a high degree of similarity between cortical responses to sAM and sFM stimuli that was reflected in both discharge rate- or synchrony-based response measures. 5) Inhibition appeared to be a contributing factor in limiting responses at modulation frequencies above the rBMF of a neuron. And 6) neurons with shorter response latencies tended to have higher tBMF and maximum discharge synchrony frequency than those with longer response latencies. rBMF was not significantly correlated with the minimum response latency.     

Auditory responses in the cochlear nucleus of awake mustached bats: precursors to spectral integration in the auditory midbrain

In the cochlear nucleus (CN) of awake mustached bats, single- and two-tone stimuli were used to examine how responses in major CN subdivisions contribute to spectrotemporal integrative features in the inferior colliculus (IC). Across CN subdivisions, the proportional representation of frequencies differed. A striking result was the substantial number of units tuned to frequencies <23 kHz. Across frequency bands, temporal response patterns, latency, and spontaneous discharge differed. For example, the 23- to 30-kHz representation, which comprises the fundamental of the sonar call, had an unusually high proportion of units with onset responses (39%) and low spontaneous rates (53%). Units tuned to 58-59 kHz, corresponding to the sharply tuned cochlear resonance, had slightly but significantly longer latencies than other bands. In units tuned to frequencies >30 kHz, 31% displayed a secondary excitatory peak, usually between 10 and 22 kHz. The secondary peak may originate in cochlear mechanisms for some units, but in others it may result from convergent input onto CN neurons. In 20% of units tested with two-tone stimuli, suppression of best frequency (BF) responses was tuned at least an octave below BF. These properties may underlie similar IC responses. However, other forms of spectral interaction present in IC were absent in CN: we found no facilitatory combination-sensitive interactions and very few combination-sensitive inhibitory interactions of the dominant IC type in which inhibition was tuned to 23-30 kHz. Such interactions arise above CN. Distinct forms of spectral integration thus originate at different levels of the ascending auditory pathway.     

Temporal coding in the frog auditory midbrain: the influence of duration and rise-fall time on the processing of complex amplitude-modulated stimuli.

1. Single-unit recordings were made in the auditory midbrain, the torus semicircularis (TS) of the northern leopard frog, to independently characterize the processing of different temporal attributes (signal duration, rise-fall time, and rate of amplitude modulation) of natural sounds and to investigate how these temporal variables interact to produce the observed responses to complex amplitude-modulated (AM) signals. Response functions, on the basis of mean spike count, were derived and categorized to describe the unit's temporal response characteristics to each of the variables. 2. To characterize the duration response functions, tone bursts of different durations (stimuli repeated at a constant repetition rate) at the unit's characteristic frequency (CF) and 10 dB above minimum threshold at CF (MT) were presented monaurally to the contralateral ear. The duration response function of a TS neuron was often related to the temporal discharge characteristics of the neuron. Increases in stimulus duration elicited an increase in spike counts (therefore, long-pass response function) from most neurons (74%) in the TS; 91% of these neurons showed tonic discharge patterns. Phasic-burst (PB) cells that were rapidly adapting showed long-pass duration response functions that were highly nonlinear, having peaks and notches embedded within the functions. On the other hand, one-third of phasic neurons tended to be insensitive to stimulus duration, giving similar spike counts in response to stimuli of greatly different durations (i.e., all pass). In the TS, some neurons (9%) only responded to a limited range of durations (i.e., band-duration pass), and still others showed a preference for shorter durations (9%; i.e., short pass); these were exhibited primarily by phasic and PB neurons. 3. To characterize the rise-fall time response functions, tone bursts having different rise-fall times were presented. The rise-fall time response functions of TS neurons had two distinct characteristics. The majority of tonic cells (91%), as well as some PB (38%) and phasic (29%) neurons, gave essentially invariant spike counts for all stimulus rise-fall times (i.e., all pass; 73% of neurons). Despite the relatively stable spike counts of neurons showing all-pass functions, the peristimulus time histograms (PSTHs) deriving from responses to slower rise-fall time stimuli exhibited a longer and somewhat more variable onset latency. About one-fourth (27%) of TS neurons, mostly phasic and PB neurons, showed higher spike counts for signals with rapid rise-fall times.(ABSTRACT TRUNCATED AT 400 WORDS)     

Lateral hypothalamus neuron involvement in integration of natural and artificial rewards and cue signals

Involvement of rat lateral hypothalamus (LHA) neurons in integration of motivation, reward, and learning processes was studied by recording single-neuron activity during cuetone discrimination, learning behavior to obtain glucose, or electrical rewarding intracranial self-stimulation (ICSS) of the posterior LHA. To relate the activity of an LHA neuron to glucose, ICSS, and anticipatory cues, the same licking task was used to obtain both rewards. Each neuron was tested with rewards alone and then with rewards signaled by cuetone stimuli (CTS), CTS1+ = 1,200 Hz for glucose, CTS2+ = 4,300 Hz for ICSS, and CTS- = 2,800 Hz for no reward. The activity of 318 neurons in the LHA was analyzed. Of these, 212 (66.7%) responded to one or both rewarding stimuli (glucose, 115; ICSS, 193). Usually, both rewards affected the same neuron in the same direction. Of 96 neurons that responded to both rewards, the responses of 72 (75%) were similar, i.e., either both excitatory or both inhibitory. When a tone was associated with glucose or ICSS reward, 81 of the 212 neurons that responded to either or both rewards and none of 106 neurons that failed to respond to either reward acquired a response to the respective CTS. Usually, the response to a tone was in the same direction as the reward response. Of 45 neurons that responded to both glucose and CTS1+, 38 (84.4%) were similar, and of 66 that responded to both ICSS and CTS2+, 47 (71.2%) were similar. The neural response to a tone was acquired rapidly after licking behavior was learned and was extinguished equally rapidly before licking stopped in extinction. The latency of the neural response to CTS1+ was 10-150 ms (58.7 +/- 40.9 ms, mean +/- SE, n = 31), and that of the first lick was 100-370 ms (204.8 +/- 59.1 ms, n = 31). The latency of neural responses to CTS2+ was 10-230 ms (68.3 +/- 53.5 ms, n = 33), and that of the first lick was 90-370 ms (212.4 +/- 58.5 ms, n = 33). There was no significant difference between the neural response latencies for the two cue tones nor between the lick latencies for the different rewards. Neurons inhibited by glucose or ICSS reward were distributed widely in the LHA, whereas most excited neurons were in the posterodorsal subarea; fewer were in the anteroventral subarea. Neurons responding to the CTS for glucose or ICSS were found more frequently in the posterior region.(ABSTRACT TRUNCATED AT 400 WORDS)     

Unit responses of the first and second somatosensory cortical areas to peripheral,thalamic, and cortical stimulation

Unit responses of the first (SI) somatosensory area of the cortex to stimulation of the second somatosensory area (SII), the ventral posterior thalamic nucleus, and the contralateral forelimb, and also unit responses in SII evoked by stimulation of SI, the ventral posterior thalamic nucleus, and the contralateral forelimb were investigated in experiments on cats immobilized with D-tubocurarine or Myo-Relaxin (succinylcholine). The results showed a substantially higher percentage of neurons in SII than in SI which responded to an afferent stimulus by excitation brought about through two or more synaptic relays in the cortex. In response to cortical stimulation antidromie and orthodromic responses appeared in SI and SII neurons, confirming the presence of two-way cortico-cortical connections. In both SI and SII intracellular recording revealed in most cases PSPs of similar character and intensity, evoked by stimulation of the cortex and nucleus in the same neuron. Latent periods of orthodromic spike responses to stimulation of nucleus and cortex in 50.5% of SI neurons and 37.1% of SII neurons differed by less than 1.0 msec. In 19.6% of SI and 41.4% of SII neurons the latent period of response to cortical stimulation was 1.6–4.7 msec shorter than the latent period of the response evoked in the same neuron by stimulation of the nucleus. It is concluded from these results that impulses from SI play an important role in the afferent activation of SII neurons.Translated from Neirofiziologiya, Vol. 8, No. 4, pp. 351–357, July–August, 1976.     

Spectral response patterns of auditory cortex neurons to harmonic complex tones in alert monkey (Macaca mulatta)

1. The auditory cortex in the superior temporal region of the alert rhesus monkey was explored for neuronal responses to pure and harmonic complex tones and noise. The monkeys had been previously trained to recognize the similarity between harmonic complex tones with and without fundamentals. Because this suggested that they could preceive the pitch of the lacking fundamental similarly to humans, we searched for neuronal responses relevant to this perception. 2. Combination-sensitive neurons that might explain pitch perception were not found in the surveyed cortical regions. Such neurons would exhibit similar responses to stimuli with similar periodicities but differing spectral compositions. The fact that no neuron with responses to a fundamental frequency responded also to a corresponding harmonic complex missing the fundamental indicates that cochlear distortion products at the fundamental may not have been responsible for missing fundamental-pitch perception in these monkeys. 3. Neuronal responses can be expressed as relatively simple filter functions. Neurons with excitatory response areas (tuning curves) displayed various inhibitory sidebands at lower and/or higher frequencies. Thus responses varied along a continuum of combined excitatory and inhibitory filter functions. 4. Five elementary response classes along this continuum are presented to illustrate the range of response patterns. 5. "Filter (F) neurons" had little or no inhibitory sidebands and responded well when any component of a complex tone entered its pure-tone receptive field. Bandwidths increased with intensity. Filter functions of these neurons were thus similar to cochlear nerve-fiber tuning curves. 6. "High-resolution filter (HRF) neurons" displayed narrow tuning curves with narrowband widths that displayed little growth with intensity. Such cells were able to resolve up to the lowest seven components of harmonic complex tones as distinct responses. They also responded well to wideband stimuli. 7. "Fundamental (F0) neurons" displayed similar tuning bandwidths for pure tones and corresponding fundamentals of harmonic complexes. This response pattern was due to lower harmonic complexes. This response pattern was due to lower inhibitory sidebands. Thus these cells cannot respond to missing fundamentals of harmonic complexes. Only physically present components in the pure-tone receptive field would excite such neurons. 8. Cells with no or very weak responses to pure tones or other narrowband stimuli responded well to harmonic complexes or wideband noise.(ABSTRACT TRUNCATED AT 400 WORDS)