Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms

1988 ◽  
Vol 60 (6) ◽  
pp. 1799-1822 ◽  
Author(s):  
G. Langner ◽  
C. E. Schreiner

1. Temporal properties of single- and multiple-unit responses were investigated in the inferior colliculus (IC) of the barbiturate-anesthetized cat. Approximately 95% of recording sites were located in the central nucleus of the inferior colliculus (ICC). Responses to contralateral stimulation with tone bursts and amplitude-modulated tones (100% sinusoidal modulation) were recorded. Five response parameters were determined for neurons at each location: 1) characteristic frequency (CF); 2) onset latency of responses to CF-tones 60 dB above threshold; 3) Q10 dB (CF divided by bandwidth of tuning curve 10 dB above threshold); 4) best modulation frequency for firing rate (rBMF or BMF; amplitude modulation frequency that elicited the highest firing rate); and 5) best modulation frequency for synchronization (sBMF; amplitude modulation frequency that elicited the highest degree of phase-locking to the modulation frequency). 2. Response characteristics for single units and multiple units corresponded closely. A BMF was obtained at almost all recording sites. For units with a similar CF, a range of BMFs was observed. The upper limit of BMF increased approximately proportional to CF/4 up to BMFs as high as 1 kHz. The lower limit of encountered BMFs for a given CF also increased slightly with CF. BMF ranges for single-unit and multiple-unit responses were similar. Twenty-three percent of the responses revealed rBMFs between 10 and 30 Hz, 51% between 30 and 100 Hz, 18% between 100 and 300 Hz, and 8% between 300 and 1000 Hz. 3. For single units with modulation transfer functions of bandpass characteristics, BMFs determined for firing rate and synchronization were similar (r2 = 0.95). 4. Onset latencies for responses to CF tones 60 dB above threshold varied between 4 and 120 ms. Ninety percent of the onset latencies were between 5 and 18 ms. A range of onset latencies was recorded for different neurons with any given CF. The onset response latency of a given unit or unit cluster was significantly correlated with the period of the BMF and the period of the CF (P less than 0.05). 5."Intrinsic oscillations" of short duration, i.e., regularly timed discharges of units in response to stimuli without a corresponding temporal structure, were frequently observed in the ICC. Oscillation intervals were commonly found to be integer multiples of 0.4 ms. Changes of stimulus frequency or intensity had only minor influences on these intrinsic oscillations.(ABSTRACT TRUNCATED AT 400 WORDS)

2003 ◽  
Vol 90 (1) ◽  
pp. 477-490 ◽  
Author(s):  
Huiming Zhang ◽  
Jack B. Kelly

Recordings were made from single neurons in the rat inferior colliculus in response to sinusoidally amplitude-modulated sounds (10-s duration) presented to the contralateral ear. Neural responses were determined for different rates of modulation (0.5 Hz to 1 kHz) at a depth of 100%, and modulation transfer functions were generated based on firing rate (MTFFR) and vector strength (MTFVS). The effects of AMPA, NMDA, and GABAA receptor antagonists were examined by releasing drugs iontophoretically through a multibarrel pipette attached to a single-barrel recording pipette. Both the AMPA receptor antagonist, 1,2,3,4-tetrahydro-6-nitro-2,3-dioxo-benzo[f]quinoxaline-7-sulfonamide disodium (NBQX), and the NMDA receptor antagonist, (±)-3-(2-carboxypiperazin-4-yl)-propyl-1-phosphonic acid (CPP) resulted in a decrease in firing rate, and the GABAA receptor antagonist, bicuculline, produced an increase in the firing rate in most of the cells examined. In some cases, the shape of the MTFFR was modified slightly by receptor antagonists, but in most cases, the peak firing rate that determined a neuron's best modulation frequency remained the same. Also there were no changes during delivery of either excitatory or inhibitory antagonists in the maximum response synchrony at the peak of the MTFVS although some changes were noticed at off-peak modulation rates particularly with the AMPA receptor antagonist, NBQX.


2006 ◽  
Vol 95 (3) ◽  
pp. 1926-1935 ◽  
Author(s):  
Liang-Fa Liu ◽  
Alan R. Palmer ◽  
Mark N. Wallace

In the auditory system, some ascending pathways preserve the precise timing information present in a temporal code of frequency. This can be measured by studying responses that are phase-locked to the stimulus waveform. At each stage along a pathway, there is a reduction in the upper frequency limit of the phase-locking and an increase in the steady-state latency. In the guinea pig, phase-locked responses to pure tones have been described at various levels from auditory nerve to neocortex but not in the inferior colliculus (IC). Therefore we made recordings from 161 single units in guinea pig IC. Of these single units, 68% (110/161) showed phase-locked responses. Cells that phase-locked were mainly located in the central nucleus but also occurred in the dorsal cortex and external nucleus. The upper limiting frequency of phase-locking varied greatly between units (80−1,034 Hz) and between anatomical divisions. The upper limits in the three divisions were central nucleus, >1,000 Hz; dorsal cortex, 700 Hz; external nucleus, 320 Hz. The mean latencies also varied and were central nucleus, 8.2 ± 2.8 (SD) ms; dorsal cortex, 17.2 ms; external nucleus, 13.3 ms. We conclude that many cells in the central nucleus receive direct inputs from the brain stem, whereas cells in the external and dorsal divisions receive input from other structures that may include the forebrain.


1997 ◽  
Vol 77 (6) ◽  
pp. 2945-2965 ◽  
Author(s):  
Adrian Rees ◽  
Ali Sarbaz ◽  
Manuel S. Malmierca ◽  
Fiona E. N. Le Beau

Rees, Adrian, Ali Sarbaz, Manuel S. Malmierca, and Fiona E. N. Le Beau. Regularity of firing of neurons in the inferior colliculus. J. Neurophysiol. 77: 2945–2965, 1997. The spike discharge regularity of 254 tonically firing units in the inferior colliculus (IC) of the anesthetized guinea pig was studied in response to tones presented at best frequency (BF) to the ear contralateral to the recorded IC. Regularity of firing was measured by calculating the coefficient of variation (CV) as a function of time over the course of a unit's response. Two hundred and fifteen units (56 under urethan and 159 under chloralose anesthesia) in the central nucleus of the IC (CNIC) were studied in detail. In response to tones at 15–25 dB above threshold, 80% of units in the urethan sample fired regularly (CV < 0.5) during their sustained response, and 46% were highly regular (CV ≤ 0.35). For chloralose the values were 68% and 23%, respectively. Units recorded under urethan were significantly more regular than those recorded under chloralose. For units in the sample with a measurable onset CV, 63% were regular and 44% highly regular under urethan, and 73% were regular and 54% highly regular under chloralose. The units' peristimulus time histogram (PSTH) patterns were classified into subdivisions of four categories: choppers [9%: chop-sustained (Cs), chop-onset (Co)]; pausers [42%: pauser-chop-sustained(P/Cs), pauser-chop-onset (P/Co), pauser-no-chop]; on-sustained(43%: primary-type, L-type, h-type); and sustained (6%). The presence of chopping was a reliable predictor of regularity: Cs and P/Cs units were highly regular throughout their response, whereas Co and P/Co units were highly regular at onset and became less regular. Some units in the other PSTH categories were highly regular despite the absence of chopping, and units with virtually identical PSTHs showed very different sustained CVs. Regularity was measured as a function of firing rate in 71 units. In 23%, regularity remained constant when firing rate changed with stimulus level. Forty-six percent fired more regularly as firing rate increased, 8% fired less regularly, and 23% of units showed no consistent relationship between CV and firing rate. Regularity did not correlate with the neurons' frequency response areas or BFs. Regular firing was also found in a smaller sample of units recorded in cortices surrounding the CNIC. We conclude that regular firing is a characteristic feature of most neurons in the IC. Regularity is a specific feature correlated with four PSTH types (Cs, Co, P/Cs, and P/Co). Other PSTH types may or may not exhibit regularity.


1995 ◽  
Vol 73 (2) ◽  
pp. 449-467 ◽  
Author(s):  
R. Snyder ◽  
P. Leake ◽  
S. Rebscher ◽  
R. Beitel

1. Cochlear implants have been available for > 20 yr to profoundly deaf adults who have lost their hearing after acquiring language. The success of these cochlear prostheses has encouraged the application of implants in prelingually deaf children as young as 2 yr old. To further characterize the consequences of chronic intracochlear electrical stimulation (ICES) on the developing auditory system, the temporal-response properties of single neurons in the inferior colliculus (IC) were recorded in deafened anesthetized cats. 2. The neurons were excited by unilateral ICES with the use of a scala tympani stimulating electrode implanted in the left cochlea. The electrodes were modeled after those used in cochlear implant patients. Responses of 443 units were recorded extracellularly in the contralateral (right) IC with the use of tungsten microelectrodes. Recordings were made in three groups of adult animals: neonatally deafened/chronically stimulated animals (192 units), neonatally deafened/unstimulated animals (80 units), and adult-deafened/prior normal-hearing animals (171 units). The neonatally deafened cats were deafened by multiple intramuscular injections of neomycin sulfate and never developed demonstrable hearing. Most of the deafened, chronically stimulated animals were implanted at 6 wk of age and stimulated at suprathreshold levels for 4 h/day for 3-6 mo. The unstimulated animals were implanted as adults at least 2 wk before the acute physiological experiment and were left unstimulated until the acute experiment was conducted. Prior-normal adults were deafened and implanted at least 2 wk before the acute experiment. 3. IC units were isolated with the use of a search stimulus consisting of three cycles of a 100-Hz sinusoid. Most units responded to sinusoidal stimulation with either an onset response or a sustained response. Onset units were the predominant unit found in the external nucleus, whereas sustained units were found almost exclusively in the central nucleus. The temporal resolution of sustained response units was measured with the use of pulse trains of increasing frequency and calculating the discharges/pulse. 4. The range of electrical pulse frequencies to which IC units responded in a temporally synchronized manner was comparable with that produced by acoustic stimulation. The discharge rate/pulse-versus-pulse frequency transfer functions of IC units were uniformly low-pass, although they varied widely in their cutoff frequencies. This variation in pulse response was partially correlated with the unit's response to sinusoids. Most onset neurons responded only to pulse frequencies below 20 pulses per second (pps). Most sustained units responded best to pulse frequencies < 100 pps, and most ceased to respond to pulse frequencies > 300 pps.(ABSTRACT TRUNCATED AT 400 WORDS)


2017 ◽  
Vol 118 (1) ◽  
pp. 544-563 ◽  
Author(s):  
Nathaniel Zuk ◽  
Bertrand Delgutte

Binaural cues occurring in natural environments are frequently time varying, either from the motion of a sound source or through interactions between the cues produced by multiple sources. Yet, a broad understanding of how the auditory system processes dynamic binaural cues is still lacking. In the current study, we directly compared neural responses in the inferior colliculus (IC) of unanesthetized rabbits to broadband noise with time-varying interaural time differences (ITD) with responses to noise with sinusoidal amplitude modulation (SAM) over a wide range of modulation frequencies. On the basis of prior research, we hypothesized that the IC, one of the first stages to exhibit tuning of firing rate to modulation frequency, might use a common mechanism to encode time-varying information in general. Instead, we found weaker temporal coding for dynamic ITD compared with amplitude modulation and stronger effects of adaptation for amplitude modulation. The differences in temporal coding of dynamic ITD compared with SAM at the single-neuron level could be a neural correlate of “binaural sluggishness,” the inability to perceive fluctuations in time-varying binaural cues at high modulation frequencies, for which a physiological explanation has so far remained elusive. At ITD-variation frequencies of 64 Hz and above, where a temporal code was less effective, noise with a dynamic ITD could still be distinguished from noise with a constant ITD through differences in average firing rate in many neurons, suggesting a frequency-dependent tradeoff between rate and temporal coding of time-varying binaural information. NEW & NOTEWORTHY Humans use time-varying binaural cues to parse auditory scenes comprising multiple sound sources and reverberation. However, the neural mechanisms for doing so are poorly understood. Our results demonstrate a potential neural correlate for the reduced detectability of fluctuations in time-varying binaural information at high speeds, as occurs in reverberation. The results also suggest that the neural mechanisms for processing time-varying binaural and monaural cues are largely distinct.


2019 ◽  
Author(s):  
Matteo Vissani ◽  
Roberto Cordella ◽  
Silvestro Micera ◽  
Luigi M. Romito ◽  
Alberto Mazzoni

AbstractBasal ganglia dysfunctions have been suggested to play a causal role in the pathophysiology of most motor and non-motor symptoms of movement disorders as Tourette Syndrome (TS) or Parkinson’s Disease (PD). Intra/post-operative recordings from the subthalamic nucleus (STN) during Deep Brain Stimulation (DBS) procedures in PD patients have highlighted specific pathological patterns of neural activity. Spatial and temporal patterns of STN neural activity in TS are still unknown due to the lack of direct microrecordings in humans. Here, we describe for the first time specific neural activities of sensorimotor STN in TS patients, as recorded during intraoperative microrecordings. We analyzed 125 single units at 0.5 mm-spaced depths from the STN of anesthetized TS patients and we observed a large fraction of units (39/125, 31.2%) intensely bursting in the delta band (<4 Hz). In anesthetized PD patients we found similar average firing rate and spectral density of STN units, but differently to TS patients, only 4/54 (7.4%) of the units displayed bursting. Remarkably, bursting units in TS STN were not homogeneously distributed over the dorso-ventral trajectory of the recording: the highest density of bursting units was reliably found at the depth for which the clinical effect was maximal. Our results provide an unprecedented characterization of STN functional architecture and single units dynamics in TS patients, paving the way to an understanding of the role of STN subterritories in TS.Key PointsSingle neuron activity in Subthalamic Nucleus (STN) of patients with Tourette Syndrome (TS) was analyzed for the first time in literature.Firing rate and spectral content of single STN neurons in TS patients were found to be similar to those of anesthetized PD patients, while the analysis of arrhythmic bursting activity revealed that in TS patients the STN is characterized by a larger fraction of bursting neurons and more intense burstsBursting activity in TS was widespread across the whole STN, but with a higher density at the optimal lead location depth for DBS


2003 ◽  
Vol 90 (5) ◽  
pp. 2818-2826 ◽  
Author(s):  
S. J. Sterbing ◽  
W. R. D'Angelo ◽  
E.-M. Ostapoff ◽  
S. Kuwada

Most sounds in the natural environment are amplitude-modulated (AM). To determine if AM alters the neuronal sensitivity to interaural time differences (ITDs) in low-frequency sounds, we tested neuronal responses to a binaural beat stimulus with and without modulation. We recorded from single units in the inferior colliculus of the unanesthetized rabbit. We primarily used low frequency (∼25 Hz) modulation that was identical at both ears. We found that modulation could enhance, suppress, or not affect the discharge rate. In extreme cases, a neuron that showed no response to the unmodulated binaural beat did so when modulation was added to both ears. At the other extreme, a neuron that showed sensitivity to the unmodulated binaural beat ceased firing with modulation. Modulation could also affect the frequency range of ITD sensitivity, best ITD, and ITD tuning width. Despite these changes in individual neurons, averaging across all neurons, the peak and width of the population ITD function remained unchanged. Because ITD-sensitive neurons also time-locked to the modulation frequency, the location and sound attributes are processed simultaneously by these neurons.


2020 ◽  
Vol 124 (6) ◽  
pp. 1706-1726
Author(s):  
Jeffrey S. Johnson ◽  
Mamiko Niwa ◽  
Kevin N. O’Connor ◽  
Mitchell L. Sutter

ML neurons synchronized less than A1 neurons, consistent with a hierarchical temporal-to-rate transformation. Both A1 and ML had a class of modulation transfer functions previously unreported in the cortex with a low-modulation-frequency (MF) peak, a middle-MF trough, and responses similar to unmodulated noise responses at high MFs. The results support a hierarchical shift toward a two-pool opponent code, where subtraction of neural activity between two populations of oppositely tuned neurons encodes AM.


1988 ◽  
Vol 60 (6) ◽  
pp. 1823-1840 ◽  
Author(s):  
C. E. Schreiner ◽  
G. Langner

1. The topographical distributions of single-unit and multiple-unit responses to amplitude-modulated tones--and to other relevant parameters of simple tonal stimuli--were defined across the main frequency representational gradient and within narrow frequency ranges represented in "frequency band laminae" in the principal midbrain auditory nucleus, the central nucleus of the inferior colliculus (ICC), in adult, barbiturate-anesthetized cats. 2. Responses to amplitude-modulated tones with the carrier set at the characteristic frequency (CF) of recorded neurons were obtained at many ICC locations in each experiment. The best modulation frequency (BMF) of neurons was defined at each site as that modulation frequency producing the highest neural discharge rate. Encountered BMFs ranged from approximately 10 to 1,000 Hz. A significant range of BMFs were recorded for neurons with any given characteristic frequency. BMF ranges varied as a systematic function of CF and of ICC recording depth. 3. Recorded BMFs were distributed topographically within functionally defined ICC frequency band laminae. Highest BMFs were found clustered in an ICC sector roughly between the middle and lateral third of its frequency band laminae. Progressively lower BMFs were recorded with increasing distance across the laminae in any direction away from the highest-BMF cluster. That is, "iso-BMF contours" were arrayed concentrically around the highest-BMF region. 4. Within frequency band laminae centered at approximately 3 and 12 kHz, quality factors (Q10 dBS) of frequency tuning curves were found to be between 0.8 and 8. Q10 dB values were distributed topographically within given frequency band laminae. Responses with narrow tuning curves (high Q10 dB values) were clustered in the middle third of the mediolateral extent of laminae; sharpness of tuning declined systematically away from this focus of highest Q10 dB values. The center of this distribution did not coincide with the center of the BMF distribution within the same lamina. 5. For neurons at greater than 90% of the ICC loci studied in these experiments, onset latencies to CF tones defined approximately 60 dB above response threshold fell within a range between 5 and 18 ms. Across a given frequency band lamina, onset latencies varied systematically, with longest response latencies recorded medially, and progressively shorter latencies recorded progressively more laterally. 6. Binaural interaction types were systematically distributed within frequency-band laminae. A cluster of excitatory-excitatory (EE) was seen, covering approximately one-third of the mapped area.(ABSTRACT TRUNCATED AT 400 WORDS)


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