Parallel mechanisms signal a hierarchy of sequence structure violations in the auditory cortex

  1. Sara Jamali
  2. Sophie Bagur
  3. Enora Bremont
  4. Timo Van Kerkoerle
  5. Stanislas Dehaene
  6. Brice Bathellier  Is a corresponding author
  1. Université Paris Cité, Institut Pasteur, AP-HP, Inserm, Fondation Pour l'Audition, Institut de l’Audition, IHU reConnect, France
  2. Université Paris Saclay, INSERM, CEA, Cognitive Neuroimaging Unit, NeuroSpin Center, France
  3. Collège de France, PSL University, France
6 figures and 1 table

Figures

Figure 1 with 2 supplements
Sequence violations are broadly signaled in the mouse auditory cortex.

(A) Sketch of the experimental setup and of the four different blocks of sound sequences. (B) Representative 1 × 1 mm two-photon imaging field-of-view with a magnification of the red rectangle. (C) …

Figure 1—figure supplement 1
Responses of synapsin-based expression of GCAMP6s to the omitted sequences in the auditory cortex.

For the two-photon imaging recordings reported in Figure 1 (synapsin-based expression of GCAMP6s), mean population activity for omitted sequences (AAAA left and BBBB right) appearing as oddball …

Figure 1—figure supplement 2
Probe localizations from Neuropixel recordings of the auditory cortex.

(A) Histological section showing the location of the probe (stained with diI, diO, or diD). (B) Reconstructed probe locations from five recordings in four mice.

Local violations selectively modulate the responses of neurons tuned to the violating sound.

(A) Sample cross-validated cluster with its d∆F/F response profile for the training (left) and test (right) sets (shading=SEM). Single-trial responses in test and training sets are shown below. (B) …

Figure 3 with 3 supplements
Modulation of sound responses by unexpected local violations is only partially due to adaptation.

(A) Sketch of the experimental paradigm. (B) (left) Trial-averaged population responses (d∆F/F) to rare and common AAAAB or AAAAA sequences (right). Same for the BBBBA and BBBBB sequences. (C) …

Figure 3—figure supplement 1
Clustering of neuronal responses for the long inter-sequence interval, dataset 1.

(A) Plot of the response profile for the 18 clusters derived from the dataset presented in Figure 3B, for the local-global with an inter-sequence interval of ~30 s. Most clusters with specific …

Figure 3—figure supplement 2
The same neurons exhibit local + global violation responses for both short and long intersequence intervals in wakefulness but not under anesthesia (although it is present at the population level).

(A) Three examples of cluster of neuron responses were tracked across three different experiments. (first column) Local + global paradigm with a short inter-sequence interval (1.5 s), (second …

Figure 3—figure supplement 3
The local + global effect is preserved across wakefulness and anesthesia.

(A) Responses of same neurons in the auditory cortex expressing GCAMP6s compared in three different experiments. (first column) Local + global paradigm with a short inter-sequence interval (1.5 s), …

Unexpected local violations produce a surprise response based on recently experienced sequence structure.

(A) (left) Heatmap of population responses of ordered single trials for two different blocks with short inter-sequence intervals (ISI) (arrows indicate rare stimuli). (right) Mean population …

Vasoactive intestinal peptide positive (VIP) interneurons signal sequence termination and omission of expected local violations.

(A) Sketch of the experimental setup. (B) Mean ± SEM population responses to the rare and common AAAAB and AAAAA sequences. Statistics for the time-averaged fifth tone response: AAAAB rare: 0.003 ± …

Parvalbumin positive (PV) interneurons weakly signal pure global violations.

(A) Sketch of the experimental setup. (B) Mean ± SEM population responses (deconvolved calcium signals) to rare and common AAAAB and AAAAA sequences, AAAAB rare: 0.058 ± 0.009% dΔF/F, AAAAB common: …

Tables

Table 1
Mean ± SEM population responses to rare (orange) and common (yellow) in classical stimulus-specific adaptation (SSA) paradigm in Figure 3.

p-values are from the statistical tests comparing between rare and common conditions (Mann-Whitney U test; n=10 for rare and n=47 for common repetitions).

Stimulus specific adaptation paradigm
Inter-stimulusintervals (second)Mean (+SEM) dAF/F rare (%)Mean (+SEM) dAF/F common (%)p-value
0.50.193 (=0.019)0.073 (+0.015)1×10–4
10.252 (+0.019)0.114 (+0.010)1×10–4
20.140 (+0.017)0.076 (+0.010)0.002
40.100 (+0.048)0.130 (+0.009)0.545
80.185 (+0.023)0.139 (+0.014)0.055
160.266 (+0.058)0.172 (+0.013)0.073

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