NL neurons project to ICcc (Takahashi and Konishi 1988
). Our results show, for the first time, that phase locking to frequencies >1 kHz in the barn owl is significantly reduced in a single step. Work in mammalian systems demonstrated a decline in the ability of neurons to phase lock through ascending auditory stations, although phase locking can still be observed as high as auditory cortex (Liu et al. 2006
; Wallace et al. 2002
; Winter and Palmer 1990
). Our results indicate that it is possible for ascending auditory centers to maintain comparable spectrotemporal tuning, in the sense of having STRFs with equal frequency and temporal tuning parameters, while discarding the phase information used by their inputs. Although a representation of phase is necessary for the computation of ITD, the many documented specializations of the early ITD pathway (Carr 1993
; Trussel 1999
) suggest that it is costly to preserve. Thus in terms of the representation of the dynamic spectral properties of the signal, it may be more efficient to maintain precision on the millisecond scale while allowing jitter to accumulate at a submillisecond scale, which would then result in a decline in phase-locking quality.
Previous studies in the barn owl (Keller and Takahashi 2000
), as well as amphibian (Hermes et al. 1981
) and mammalian models (Carney and Yin 1989
), demonstrated patterned (that is, stimulus-locked) responses in the midbrain using broadband noise. However, because of the segregation of sound localization cues in the barn owl, it is not immediately clear whether these responses emerge from the ITD pathway or the ILD pathway. Taken all together, our results suggest that the population activity of the nuclei of the ITD pathway, and specifically ICcc, can be treated as a dynamic spectrum analyzer with a temporal resolution of approximately a millisecond. Although this does not rule out any role of the ILD-sensitive neurons in the generation of spectral tuning in higher auditory centers, it does argue against the possibility that the spectrotemporal tuning in ICls neurons reported by Keller and Takahashi (2000)
is attributed solely to the inputs from the ILD-sensitive neurons.
We did not examine the effect on the STRF of varying ITD because the rectification and large dynamic range of the rate-ITD functions of ICcc neurons (Christianson and Peña 2006
) made collecting a sufficient number of spikes for nonpeak ITDs prohibitive. However, raster plots from the work of Carney and Yin (1989)
indicate that the timing of spikes, if not their number, is relatively invariant to changes in the ITD in the cat IC; this is confirmed by the work demonstrating that spike timing does not appear to convey information related to the ITD (Chase and Young 2006
). Previous work in owls (Keller and Takahashi 2000
) demonstrated that STRFs of neurons in the ICls, to which ICcc projects, are also invariant under changes in ITD. Thus any dependency on ITD of STRFs for NL and ICcc neurons is likely to be explainable by a modulation in gain resulting from the dependency of mean firing rate on ITD.
In previous work, we showed that the transition from NL to ICcc acts as a noise-elimination phase in the representation of ITD (Christianson and Peña 2006
). It might be expected that this improvement in the encoding of a spatial location cue might come at the expense of the representation of the spectral content; this is especially true in the barn owl, where it is established that there is a frequency convergence to resolve ITD coding ambiguity (Mazer 1998
; Saberi et al. 1999
; Takahashi and Konishi 1986
). Here, we demonstrate that this is not the case. The conclusion is thus that the pooling that produces the reduction in ITD encoding noise must occur over a population of NL neurons with extremely similar spectrotemporal tuning. This may not be as difficult to arrange as it may appear. Theoretical work suggests that the neurons that compute the ITD should behave as cross-correlators (Licklider 1959
), which experimental work supports (Yin and Chan 1990
). One of the properties of cross-correlation is that the shape of the cross-correlation function (in this case, the rate-ITD function) should be determined by the spectral tuning of the cross-correlator, known as the Wiener–Khinchin relationship. Although the experimental evidence in support of this property is weak (Yin and Chan 1990
), it suggests that with an assumption of a moderate degree of homogeneity in the properties of NL neurons, the expectation would be that similar spectral tuning should accompany similar ITD tuning.
At first glance, the observation from Christianson and Peña (2006)
that NL neurons are noisy compared with ICcc neurons would seem to be in conflict with our observation that the variability in response to frozen noise stimulation was the same in both nuclei. In fact, the noise in the NL rate-ITD functions is likely to be the result of the spectrotemporal tuning itself. Because white noise has a uniform spectrum only when averaged over time, we would expect the firing rate over small time windows to be influenced to a large degree by the instantaneous power spectrum of the signal. The result that the STRFs and the SACs of both NL and ICcc neurons are similar suggests that the variability in response arising from spectral properties of the signal is the same in both nuclei, and we have observed that the overall variability in firing rate as a function of mean firing rate was similar in both NL and ICcc (Christianson and Peña 2006
). Thus it is likely that a primary source of “noise” in the rate-ITD function is a result of the variations in spike timing linked to spectrotemporal attributes of the sound, which is consistent with work done in cats indicating that ITD information is not carried by precise spike timing (Chase and Young 2006
). However, in ICcc the increase in overall dynamic range in the rate-ITD function (Christianson and Peña 2006
) allows that the variation in mean firing rate resulting from the firing patterns related to the spectral properties of different signals with the same ITD be small compared with the variation in mean firing rate resulting from changes in the ITD. As such, this constitutes an elegant implementation of simultaneous rate- and timing-based coding strategies to represent multiple stimulus parameters within the limited language of neuronal spiking.