3.1. Response Areas, Response Properties, and Histograms
to show representative response areas, PSTHs, rate and first spike latency curves, and ISIHs for units from all three monkey species of the 8 response types commonly used to describe CN neurons. The CV vs time is plotted with each PSTH, and indicated for each ISIH distribution. Noise RCs are included if obtained (col. 3). illustrates the response measures for three chopper units, a chopper with widely spaced PSTH modes (Cw) and a Cs unit from the squirrel monkey, and a Ct unit from the marmoset.
Figure 1 RA (1st col.), PSTH with unit ID (2nd col.) and CV (red line), CF rate (black line) with noise rate curve (green line) and latency (red line) curves (3rd col.), and ISIH with CV value (4th col.) for 3 CN units. From the top down, squirrel monkey unit (more ...)
Figure 3 RA (col. 1), PSTH with CV (col. 2), rate, noise rate, and latency curves (col. 3), and ISIH with CV value (col. 4) for PL units isolated in each species. From the top down, cynomolgus unit CM04-15 had a CF of 1.1 kHz, squirrel monkey unit SM09-28 had (more ...)
SM04-4 (top row, ) was a Cw unit with a CF of 3.9 kHz, SR of 1 spike/s, TH of 29 dB, and Q10 of 1.9. This chopper-wideband classification is based on the large mean interspike interval of nearly 11 ms between the modes in the PSTH. The unit displayed monotonic pure tone and noise RCs, and had a DR of 65 dB and latency at CF of 4.4 ms. SM04-4 did not phase lock well to low-frequency tones, and the maximum SC observed throughout the RA was 0.41. No MTF was established for this unit. Based on the penetration reconstruction, it is likely that SM04-4 was located in the DCN. Over an approximately 1 mm path, the electrode isolated units whose CFs progressively declined from about 7.5 kHz to below 1 kHz. The response type sequence of the isolated units was PL, buildup (B), Cw, pauser-buildup-chopper (PBC), and two OnCs.
SM01-12 (2nd row, ) was a Cs unit with a CV < 0.3, a CF of 3.3 kHz, SR of 2 spikes/second, TH of 30 dB, and Q10 of 3.2. The unit displayed a monotonic rate curve with a DR of 35 dB and latency at CF of 5.8 ms. The magnitude of phase locking was insignificant throughout its RA. No MTF was obtained for SM01-12. Based on the penetration reconstruction, it is likely that SM01-12 was located in the PVCN. Over a short electrode path of less than 500u below the CN surface, a Cw, 2 PLns, and a Cs unit were isolated in sequence. CFs for these units ranged from 2.4 – 4 kHz.
MM01-109 (3rd row, ) was characterized as a Ct unit and had a CF of 5.3 kHz, SR of 15 spikes/second, TH of 28 dB, and Q10 of 6.6. The unit displayed a monotonic rate curve with a DR of 50 dB and 6.3 ms latency at CF. The unit phase locked well at lower frequencies with the maximum SC of 0.89 throughout the RA. A MTF was also obtained for this unit that showed decreasing SC values at higher SPL levels of AM modulation. Maximum MTF-SC values for this unit were 0.7 at 30 dB, 0.5 at 50 dB, and 0.3 at 60 dB, and it had a cutoff frequency of 200 Hz. The shape of MM01-109’s MTF was lowpass. Based on the penetration reconstruction, MM01-109 was likely located in the AVCN. Over an electrode excursion of approximately 1800µm, 2 PL units were encountered, and then 6 Ct units. During this recording sequence, CFs progressively declined from 14.5 to 3.5 kHz.
documents OnC, OnI, and PLn units from the squirrel monkey; these units are shown together because onset activity is the predominant feature in each response category. The top row of illustrates responses from SM02-32, an OnC unit. SM02-32 had a CF of 1 kHz, SR of 7 spikes/second, TH of 23 dB, and Q10 of 1.6. The unit had monotonic tone and noise RCs and had a DR of about 70 dB and a latency of 5.0 ms. The response map shows broad tuning, as indicated by the low Q10 of 1.6 that is typical of OnC units. The SC was 0.18 at CF, while the maximum SC obtained over the entire RA was 0.84. No MTF was obtained from this unit. Based on the penetration reconstruction, it is likely that SM02-32 was located in the PVCN. Over an electrode excursion of approximately 1500 µm, 1 Ct unit, an On unit, the OnC unit, 2 Ct units, and 3 PL units were encountered. During this recording sequence, CFs were 7 kHz and 4.6 kHz for the Ct and On units, and then dropped to below 1.7 kHz for the remaining units isolated.
Figure 2 RA (col. 1), PSTH with CV (col. 2), rate, noise rate, and latency curves (col. 3), and ISIH with CV value (col. 4) for 3 CN units with a prominent initial peak in their PSTH. From the top down, squirrel monkey unit SM02-32 was classified as an OnC unit, (more ...)
The second row in shows SM01-8, a PLn unit. SM01-8 had a CF of 2.5 kHz, SR of 74 spikes/second, TH of 21 dB, and Q10 of 3.8. The unit displayed monotonic tone and noise RCs, approximately a 30 dB DR and a latency of 2.7 ms. The SC was 0.05 at CF, and the maximum SC of the MTF was 0.36. The shape of SM01-8’s MTF was bandpass. Unit SM01-8 was located approximately 1500 µm below the brain surface, and since no other units were isolated in this penetration, we cannot determine its location within the CN complex.
The third row of shows SM09-7, an OnI unit. SM09-7 had a CF of 10 kHz, SR of 3 spikes/second, TH of 25 dB, and Q10 of 4.2. The unit had monotonic tone and noise RCs and a DR of about 30 dB. The latency for SM09-7 was 3.0 ms, and it was broadly tuned. The PST SC was insignificant at CF, but the highest SC within the RA was 0.83. Based on a dorsal-to-ventral penetration reconstruction plotting unit electrode depth vs CF, we believe SM09-7 might have been located in the PVCN. Over an electrode excursion of less than 800µm, 3 Ct units, 1 OnI unit, and 2 units that could not be classified were encountered. CFs for the 6 units isolated were in the 7.8 to 23 kHz range, with no consistent tonotopic pattern.
shows data from PL units isolated in each species, and includes PL neurons with low, middle, and higher CFs. The top row illustrates CM04-15, a PL unit with a CF of 1.1 kHz, SR < 1 spike/second, TH of 52 dB, and Q10 of 2.4. The unit displayed a monotonic rate curve with a dynamic range of about 35 dB, and had a latency of 5.5 ms. As is clear from the ISIH, the unit tightly encoded the stimulus waveform at lower frequencies. The maximum SC at CF was 0.79, and the maximum SC throughout RA was 0.9. No MTF was obtained from this unit. Based on the penetration reconstruction, it is likely CM04-15 was located in the AVCN. After traveling about 1 mm, the electrode isolated four neurons over approximately 450 um, including 3 PL and 1 OnC units. The PL units had CFs between 1.0 and 1.6 kHz, and the OnC’s CF was 3.4 kHz.
The second row documents responses from SM09-28, a PL unit with a CF of 1.8 kHz, SR of 8 spikes/second, TH of 37 dB, and Q10 of 2.3. The rate curves at CF and using noise were monotonic, and the minimum latency at CF was 3.9 ms. The maximum SC at CF for this PL unit was 0.51, while the maximum SC at lower frequencies in the RA was 0.95 and its maximum MTF-SC was 0.59. The shape of the MTF was lowpass. The dorsal to ventral penetration reconstruction also indicates SM09-28 was likely located in AVCN. Here, 2 Ct units with CFs of 10.2 and 7.4 kHz were isolated about 700 um below the brain surface, and then 6 PL units were found over the next 700 um. CFs for the 2 most dorsal PL units were 8.0 kHz, and then dropped from 1.8 kHz for sm09-28 to around 600 Hz for the remaining 3 PL units.
The last row in shows MM01-15, a PL unit. MM01-15 had a CF of 6.8 kHz, SR of 42 spikes/second, TH of 17 dB, and Q10 of 5.4. The unit displayed a monotonic rate curve and had a DR of about 20 dB and a latency of 2.9 ms. MM01-15 did not phase lock well, and its MTF-SC was 0.06. Iso-intensity RA curves for MM01-15 also demonstrated inhibitory side bands on both sides of CF (see Methods).
Based on a dorsal-to-ventral reconstruction of the penetration plotting unit electrode depth vs CF, we believe MM01-15 might have been located in the AVCN. Over an electrode excursion of approximately 1600 µm, 12 neurons were isolated, including 7 PL, 3 PLN, 1 P, and 1 unclassified unit. During this recording sequence, the first 2 CFs (PLn and PL units) were around 6 kHz. The next 5 CFs (4 PL and 1 unclassified unit) jumped to 25 – 32 kHz, and the remaining CFs (2 PLn and 3 PL units) decreased from 6.8 to 0.9 kHz.
3.2. Chopper Responses
illustrates one marmoset unit () and three squirrel monkey units categorized as Cts (), and one squirrel monkey unit classified as a Cw (). Note that the PSTH was shortened to 30 ms here for presentation purposes, but the response patterns illustrated in the first 30 ms continued throughout the tone burst stimuli. PSTHs from these units clearly demonstrate they were chopper units, and the ISIHs reflect distributions typically associated with Ct and Cw units. CV values were highest for the first three Ct units shown and lowest for the Cw unit, indicating a very regular discharge rate throughout the stimulus for the Cw neuron. The chopper in would be labeled Cu by the criteria of Young et al. (1988)
, i.e. a constant mean rate and decreasing CV as a function of time.
Figure 4 Post stimulus time (left) and interspike interval (right) histograms from four Ct (A–D) and one Cw (E) units in the squirrel monkey and marmoset (A). Characteristic frequency, spontaneous rate, threshold and coefficient of variation for the ISIH (more ...)
3.3. Distribution of Response Types
There were sufficient data for 296 units to determine response type. summarizes the number of categorized units recorded for each species, and the percentage each response type represents for all monkeys combined. If data from the three monkey species are combined, Cw, Ct, and Cs units constitute approximately 36% of all units recorded, On, OnC, and OnI units about 10%, and PL and PLn units about 47%. DCN unit types (i.e. Cw, P, and “all other” units) accounted for about 12% of the neurons isolated. It is not possible to assess whether these recordings forma representative sample.
Table 1 The number of units of each response type in each monkey sub-species (number of subjects ) and the percentage each response type represents for all species combined. Response types typically associated with the DCN (i.e. P/C, PBC, B, and Types 2, IV, (more ...)
Based on the division of chopper response patterns by CV (i.e. CV values for Ct units are >0.3 and <0.3 for Cs units), there were fewer Cs than Ct units. As discussed in Methods, whether those units with a lower firing rate with CVs <0.3 should be classified as Cw or Ct units is problematic. Cw classification has been reserved for choppers found in the DCN with a maximum discharge rate less than 100 spikes/s. There were 84Ct, 5 Cs and 17 Cw units using a CV criterion of 0.3.
3.4. Descriptive Statistics for Response Types in Primate Species
If at least 5 neurons of a response type were recorded and a particular response parameter was obtained (typically on a subpopulation of the number of cells categorized within a response group), descriptive statistics for those cells in each monkey species are shown in –. These include mean and standard deviation (SD) values for SR, TH, DR, PST-SC, and MTF-SC. Note that because phase locking significantly decreases at higher frequencies (see e.g. below), these tables only include PST SC values derived from neurons with CFs ≤ 2 kHz.
Table 2 Mean and (SD) of several descriptive statistics for 3 response types of marmoset CN neurons. The number of units of each response type is shown (top row). Mean and standard deviation reported for each was typically done on a subpopulation of the N in (more ...)
Primate auditory-nerve fiber spontaneous rate data from published and unpublished data.
Figure 6 (A) Q10 = CF/bandwidth at 10 dB above threshold on a log-log scale, (B) latency, (C) maximum synchronization coefficient from the PSTH at CF, (D) maximum MTF synchronization coefficient, (E) thresholds in dB, and (F) spontaneous rates in spikes/s for (more ...) 3.4.1. Marmoset
Because the number of Ct and PL units studied in the marmoset is substantially higher than PLn neurons, it is most useful to compare their response values. These two populations did not show significant differences with regard to SR, TH, Q10s or DR. While only 2 Ct and 3 PL units had CFs ≤ 2 kHz, the PL units appeared to phase lock significantly better to short tone bursts at CFs. However, MTF-SCs were determined for 22 Ct and 22 PL units in the marmoset, and both those population types were able to phase lock well to the waveform envelop of AM stimuli.
3.4.2. Cynomolgus macaque
Most data from the Cynomolgus macaques were derived from a single animal, and thresholds increased during that experiment. PL units were the largest population studied (27), and OnC (6) and On (5) categories the next most populous. Average spontaneous rates were 38.7 sp/s for PL units, 44.9 sp/s for OnC’s, and 16.1 sp/s for On units. Of the 27 PL neurons isolated, 12 had CFs ≤ 2 kHz. As in the marmoset, these low frequency PL units phase-locked well to short tone bursts at CF, and their mean PST SC at CF was 0.64. Only 1 MTF-SC value could be obtained; that value was 0.74, and it was obtained from a PL unit with a CF of 18 kHz. TH values are not included because of the changes observed during the best experiment.
3.4.3. Squirrel monkey
The squirrel monkey experiments yielded the largest amount of data. Here, PLn and Ct units had substantially higher SRs than Cw, On, and OnC response types, but TH values for these 6 response types did not appear to be significantly different. OnC units had the lowest Q10 values and the highest DR, but these values are based on a limited sample of 8 neurons.
Cw, Ct, PL, and PLn neurons were the largest populations isolated in the squirrel monkey. Here, 7 Ct, 23 PL, and 3 PLn units had CFs ≤ 2 kHz, and PST SCs for the PL response groups appeared to be much higher than the CT cells (single sided t-test P < .005). For each of these 6 response types shown in , MTF-SC values indicated these cell types could clearly encode the envelop of an AM stimulus. This MTF-SC parameter population included 3 Cw, 27 Ct, 2 OnC, 7 PL, and 4 PLn cells; a single On unit had a MTF maximum SC of 0.88.
Table 4 Summary spontaneous rate, threshold, and synchronization coefficient values from PST histograms and MTFs as derived from squirrel monkeys and marmosets. Threshold values exclude 3 Cw, 2 OnC, and 2 PL units in the squirrel monkey with thresholds ≥ (more ...)
3.5. Temporal Modulation Transfer Functions for Different Response Types
show the temporal modulation transfer function synchronization coefficients as a function of AM modulation frequency for six example Ct, PL, and PLn units, and are taken from squirrel monkey and marmoset neurons. The MTFs for chopper units illustrate both lowpass (A) and bandpass (B) characteristics that either maintained (A,B) or changed (C) that form over the 40 dB intensity range. Most choppers had a lowpass MTF shape (41 of 59, 69%). Those classified as bandpass were usually lowpass at low intensities and became bandpass by 50 to 70 dB SPL. Bandpass center frequency was usually between 200 and 800 Hz, with 300 Hz occurring most often, although the Ct unit in had a bandpass MTF at all intensities with a very low center frequency (~ 100 Hz). Cutoff frequencies of the MTFs were estimated as the frequency where the magnitude of the MTF dropped below 0.2, and these ranged from 200 to 1000 Hz, with the majority below 500 Hz.
Figure 5 Modulation transfer function synchronization coefficients of 3 example Ct (A–C), 2 PL (D, F), and PLn (E) neurons at 30 dB (thin line), 50dB (medium line), and 70dB (heavy line) plotted as a function of AM modulation frequency. CFs of individual (more ...)
Primarylike units more often had MTFs that were lowpass (). The exceptions were PLn units that often had bandpass MTFs (). Some PL units had a bandpass MTF at high levels ().
The maximum MTF-SCs exceeded 0.5, which is the value that would be expected if the modulating waveform were reproduced by the instantaneous firing pattern. Another point to note is that as intensity is increased the magnitude of the MTF remains high, thereby preserving the temporal code. While the magnitude of the MTF typically decreased with increasing intensity for both choppers and primarylike units, the decrease was small for the Ct unit in and the PLn unit in . In other words, a robust temporal code is preserved in some units. In contrast, the rate-MTFs (not shown) were nearly uniformly flat and increased with intensity for choppers and primarylike units. Therefore, there is no AM coding in the average discharge rate of these unit types.
3.6 Distribution of Response Properties for Selected Response Types
summarizes the total population of neurons encountered during these experiments, and – show the actual distribution of Q10, latency, PST-SC, MTF-SC, threshold, and spontaneous rate values for the seven largest subpopulations of response types from this table. These include: Cw units from the squirrel monkey, Ct units from the marmoset and squirrel monkey, PL units from all three subspecies, and PLn units from the squirrel monkey. Since some of these response properties were not obtained for all units, – only illustrate data if at least 4 values were derived for each property.
Figure 9 (A) Q10, (B) latency, (C) synchronization coefficient, (D) maximum synchronization coefficient from MTF, (E) thresholds in dB, and (F) spontaneous rates in spikes/s for PLn units in the squirrel monkey (♦) and marmoset (□). Only 4 MTFs (more ...)
shows the distributions of Q10, latency, PST-SC, MTF-SC, threshold, and spontaneous rate values for CT units recorded in the marmoset and squirrel monkey. The MTF-SC value is the maximum SC value observed over the range of AM modulation frequencies, which was usually varied from 50 or 100 – 2550 Hz in 100 Hz steps. Regression lines have been fitted to the latency data from both species in , with outliers exceeding 8 ms excluded (i.e. 1 point in the squirrel monkey and 3 in the marmoset). The shape of the resulting curves are similar to those observed in other animals. Ct cell latencies decrease approximately 2 ms as CFs are increased from 500 Hz to 30 kHz. Threshold distributions () are similar for both species while squirrel monkey cell spontaneous rates are somewhat lower than those of marmoset CT cells ().
displays the distribution of Q10, latency, threshold, and spontaneous rate for Cw units in the squirrel monkey. Only 2 units could be assigned PST SC values and 3 units MTF values, so those data are not included here.
(A) Q10, (B) latency, (C) threshold, and (D) spontaneous rate data for low discharge rate Cw units in the squirrel monkey.
show the distribution of Q10, latency, PST-SC, MTF-SC, threshold, and spontaneous rate values for PL units recorded in the squirrel monkey, marmoset, and cynomolgus macaque. The latency values in were obtained from rate curves derived from the RA at CF, and a regression line has been fitted to the combined data from the three species. Here, latencies for PL units with characteristic frequencies down to 500 Hz are approximately 4.5 ms, and decrease to approximately 2.5 ms for PLs with characteristic frequencies greater than 30 kHz. Squirrel monkey SCs () are somewhat lower than for the other species. SCs are nearly zero by 4 kHz in all species. The temporal modulation function SCs have an especially wide range from 0.25 to 0.95 in the region of 10 kHz CFs. Thresholds were higher in the macaques, and as explained in Methods, this might be due in part to calibration difficulties in this species. Spontaneous rates were higher in marmosets than squirrel monkey (single-sided t-test, P < 0.05 while the two-sided t-test yielded P < 0.1).
Figure 8 (A) Q10, (B) latency, (C) synchronization coefficient from PSTH at CF, (D) maximum MTF synchronization coefficient values, (E) thresholds in dB, and (F) spontaneous rates in spikes/s for PL units in the squirrel monkey (♦), cynomolgus macaque (more ...)
shows the distribution of Q10, latency, PST SC, MTF-SC, threshold, and spontaneous rate values for PLN units recorded in the squirrel monkey and marmoset. The latency values in were obtained from rate curves derived from the RA at CF. A regression line has been fitted to the combined data from both species, but the two highest points just above a CF of 20 kHz were excluded from the fit. Here, latencies for PLn units are approximately 3.5 ms for neurons with characteristic frequencies near 500 Hz, and drop to approximately 2 ms for PLns with characteristic frequencies above 20 kHz. The average spontaneous rate (F) is nearly 50 spikes/s.
3.7. Summary Statistics for Three Primate Species
In , we have combined response parameter values derived from the 7 largest response categories in squirrel monkeys and marmosets (see ), and each response type contained a minimum of 5 units. Response parameter values shown are SR, TH, PST SC for units with CFs <= 2 kHz, and MTF-SC. SD values were calculated only if at least 5 values were available for that particular response parameter.
When data are combined, three features from the data set appear to be the most salient:
- units in the general onset category (i.e. On and OnC units) have a lower SR than found in the other major response groups.
- For units with CFs <= 2 kHz, PL neurons phase lock much better than CT cells.
- Cw, Ct, PL and PLn response types appear to encode the waveform envelop well, as measured by the MTF-SC value. It is also worth noting that although MTF-SC values were determined in a total of 9 other units in the On, OnC, and P categories, the lowest mean MTF-SC for those small populations was 0.74.