Human neurons discriminate fine sound frequencies as well as bats

A short paper in this week's Nature finds that neurons in the human auditory cortex have an unusual capacity for perceiving small frequency differences:

Just-noticeable differences of physical parameters are often limited by the resolution of the peripheral sensory apparatus. Thus, two-point discrimination in vision is limited by the size of individual photoreceptors. Frequency selectivity is a basic property of neurons in the mammalian auditory pathway. However, just-noticeable differences of frequency are substantially smaller than the bandwidth of the peripheral sensors. Here we report that frequency tuning in single neurons recorded from human auditory cortex in response to random-chord stimuli is far narrower than that typically described in any other mammalian species (besides bats), and substantially exceeds that attributed to the human auditory periphery. Interestingly, simple spectral filter models failed to predict the neuronal responses to natural stimuli, including speech and music. Thus, natural sounds engage additional processing mechanisms beyond the exquisite frequency tuning probed by the random-chord stimuli.

The similarity with bats reminds me of a number of papers about FoxP2 -- although this is a totally different pathway. Is it about language?

This paper is totally full of jargon and extraordinarily difficult to read (and frequent readers know I wouldn't say that lightly!).

The main features are:

1. this is about the sensitivities of neurons in the auditory cortex of the brain, not anything about the ears or auditory nerves;

2. their mammalian comparisons include macaques but not apes, so it is not evident that this relates to recent human evolution (although it may);

3. the neuron responses seem to explain actual sensory acuity in humans:

These results are relevant to the apparent paradox of frequency hyperacuity demonstrated repeatedly in human psychoacoustics. Subjects with normal hearing, even untrained, successfully detect spectral differences substantially narrower than the presumed bandwidth of single auditory nerve fibres. Our results demonstrate that frequency differences smaller than 3% could be reliably detected from single-trial responses of single units in human auditory cortex. This value is comparable to the minimum detection threshold reported in untrained subjects. Thus, the responses of one of these cortical neurons could, in principle, underlie behavioural performance on a single-trial basis. Tramo et al. reported that bilateral lesions of human auditory cortex cause significant elevations in frequency discrimination thresholds, suggesting a functional role for the electrophysiological findings reported here.

4. the paper mentions that auditory fine-tuning may be related to language ability. In a press release, one of the authors suggested that the fine-tuning may be at too fine a level to be useful for language:

"This is remarkable selectivity," said Fried, who is also the co-director of UCLA's Seizure Disorder Center. "It is indeed a mystery why such resolution in humans came to be. Why did we develop this? Such selectivity is not needed for speech comprehension, but it may have a role in musical skill. The three percent frequency differences that can be detected by single neurons may explain the fact that even musically untrained people can detect such frequency differences."

I wouldn't be so quick with this interpretation. People may comprehend language despite many hearing challenges, but that doesn't mean there was no selection on hearing in association with language. Besides, speech includes a wide array of auditory information beyond words. The tonal qualities of a person's voice enable individual recognition. The fine tonal differences in a single person's speech indicate qualities such as emotional state. Plus, there are tonal languages, which may also advantage the perception of small pitch differences.

5. The last paragraph of the paper puts the auditory cortex into the context of other brain regions which have been found to have highly sensitive coding of responses in single neurons:

Previous studies in alert human subjects have shown very selective responses in single neurons from other brain areas. Notably, Quiroga et al. reported highly specific responses to individual people or landmarks from a subset of medial temporal lobe neurons, suggesting an invariant, sparse code. The high selectivity reported here may be a counterpart of the same phenomenon, resulting in a sparse coding of frequency in auditory cortex. We can only speculate why a low-level cue such as frequency is represented so explicitly and predominantly in single neurons of human auditory cortex but not in the auditory cortex of other terrestrial mammalian species.

This seems like a very interesting trend in brain research. New equipment and instrumentation allows researchers to register the outputs of single neurons, which explains why these kinds of results keep coming up recently.

If various kinds of brain processing are really organized into so-called "sparse arrays," we may need to re-evaluate the importance of gross anatomical features like brain size or the relative sizes of different brain areas. Very tiny levels of organization within brain regions may explain much of human brain evolution, with overall size -- or even the size of local regions -- being secondary.

This study also reminds us that selection on a complex structure like the brain may be accomplished along many different dimensions. Here, we see a change in the function of individual neurons, possibly enabled by local organization that functionally differentiates different neurons from each other. This is irrespective of larger structural changes to the auditory cortex, the size of the auditory cortex relative to other brain regions, the extent of lateralization of processing, or the size of the brain overall. It is also irrespective of the auditory nerve, the cochlear cells that receive sound, and the rest of the structures that influence acoustic properties of sound. Yet, every single one of those other pathways might also be targets of selection related to auditory processing; some stronger, and some weaker.

So it should be no wonder that it is hard for geneticists and neuroscientists to work these things out!

References:

Bitterman Y, Mukamel R, Malach R, Fried I, Nelken I. 2008. Ultra-fine frequency tuning revealed in single neurons of human auditory cortex. Nature 451:197-201. doi:10.1038/nature06476