Primary Cortical Representation of Sounds by the Coordination of Action-Potential Timing

Primary Cortical Primary Cortical Representation of Sounds Representation of Sounds

by the Coordination of by the Coordination of Action-Potential Timing Action-Potential Timing

R. Christopher deCharms & Michael M. R. Christopher deCharms & Michael M. MerzenichMerzenich

Take-home: “Population coding based on relative spike timing can systematically signal stimulus features, it is topographically mapped, and it follows the stimulus time course even where mean firing rate does not.”

RationaleRationale

Cortical population coding is still not understood.Cortical population coding is still not understood.Firing rates versus relative timing of firingFiring rates versus relative timing of firingChanges in firing rates of most neurons do not Changes in firing rates of most neurons do not reflect duration of a stimulus.reflect duration of a stimulus.Sensorimotor neurons in frontal cortex change Sensorimotor neurons in frontal cortex change the relative timing of firing even when firing rate the relative timing of firing even when firing rate does not change.does not change.Purpose: Investigate the role of relative action Purpose: Investigate the role of relative action potential timing in population coding of stimuli in potential timing in population coding of stimuli in the primary auditory cortex.the primary auditory cortex.

MethodsMethods

3 marmoset monkeys3 marmoset monkeysExtracellular recordings from pairs of locations of Extracellular recordings from pairs of locations of neurons in the supragranular primary auditory cortex 75-neurons in the supragranular primary auditory cortex 75-1,000 µm apart1,000 µm apartComputer sampling at 20 kHz and spike sortingComputer sampling at 20 kHz and spike sortingThresholded signals gave 54 pairs of single units & 369 Thresholded signals gave 54 pairs of single units & 369 pairs of multiunit groupspairs of multiunit groupsAuditory stimuli produced by a DSP chip and presented Auditory stimuli produced by a DSP chip and presented binaurallybinaurallyStatistical significance est. between cross-correlogramsStatistical significance est. between cross-correlogramsMean, s.e. & confidence limits derived from all trials Mean, s.e. & confidence limits derived from all trials (~100)(~100)

Question 1Question 1

Do cortical neurons that fire at low rates Do cortical neurons that fire at low rates provide information about stimuli?provide information about stimuli?

Figure 1Figure 1

f & g: mean firing rates at the 2 locations

a–d: average cross-correlations between 2 locations (100 reps.)

e: amplitude envelope; 70 dB at 4 kHz; pure-stimulus tone

f & g: firing-rate response to a long-lasting stimulus similar to a brief 50 ms stimulus

b & c: the change in coordinated rate was highly significant (P<1x10-5 for b, P>3x10-4 for c, permutation test)

d: Control for remaining relative spike timing or short-term synaptic plasticity after the introduction of a stimulus: unchanged

Conclusion: “Cortical neurons can thus maintain signals about ongoing stimuli by temporally coordinating the few action potentials present even at low firing rates.”


Is neuronal coordination effective at the Is neuronal coordination effective at the level of individual pairs of neurons or at level of individual pairs of neurons or at the population level?the population level?

Figure 2Figure 2a: single pair of neurons: increased cross-correlation during the stimulus, but variability too high

b: single pair of neurons with a significant cross-correlation, but little or no change in tonic firing rate

c: comparison of two groups of well-isolated units with similar effect to b, but more robust

d: two thresholded multiunit groups; similar effect as in c

e: single unit and the local field potential (adjacent electrode): increase in correlation with sound

Conclusion: “Neuronal coordination is a population effect.”


Is neuronal coordination stimulus specific, Is neuronal coordination stimulus specific, and if so, how is this specificity and if so, how is this specificity represented on the cortex?represented on the cortex?

Figure 3a-h: frequency tuning of spike time coordination between two groups of neurons

Coordinated rate of action potentials was increased significantly by a 4 kHz stimulus & significantly decreased by a 6.35 kHz stimulus

3e: coordination rate increases even when mean firing decreasesConclusion: “ Where firing rate and relative timing both change, the absolute number of coordinated events reflects both effects.”

Figure 3 Figure 3

i-k: spatial locations on auditory cortex

Red: increased coordinated rate

Blue: decreased coordinated rate

4 kHz

70 dB

4 kHz

40 dB

2.52 kHz

40 dB

Center frequency of tonic phase coordinated spike rate tuning

Conclusion: Topographic map of coordinated spike tuning reflects the map for traditional onset burst tuning.


Does neuronal coordination mimic the Does neuronal coordination mimic the duration of the stimulus at locations where duration of the stimulus at locations where the firing rate does not?the firing rate does not?

Figure 4Figure 4

b & c: no significant change in firing rate at the same two locations as in a (not even transients)

a: coordinated discharge rate at two locations

e: mean plus s.e. of all the coordinated spike-rate time courses

f: average of all individual firing rates from same population as in e

Conclusion: “…a target location which samples across a broad & non-homogeneous population of neurons that are firing on average near background rate can nonetheless extract the time course of an ongoing stimulus by using temporal coincidence information from that population.”

ConclusionsConclusions

At stimulus transients, population firing rate & At stimulus transients, population firing rate & coordinated firing rate both reflect the change in coordinated firing rate both reflect the change in signalsignalResults reveal that relative spike timing of action Results reveal that relative spike timing of action potentials in the primary auditory cortex may be potentials in the primary auditory cortex may be vital for signaling features of a stimulus once vital for signaling features of a stimulus once population firing rate has returned to baseline. population firing rate has returned to baseline. More basic than the concept of neuronal More basic than the concept of neuronal groupinggroupingEvolving temporal pattern of activity Evolving temporal pattern of activity

Primary Cortical Representation of Sounds by the Coordination of Action-Potential Timing

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