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Internally organized mechanisms of the head direction sense.

Peyrache A, Lacroix MM, Petersen PC, Buzsáki G - Nat. Neurosci. (2015)

Bottom Line: The temporal correlation structure of HD neurons was preserved during sleep, characterized by a 60°-wide correlated neuronal firing (activity packet), both within and across these two brain structures.During rapid eye movement sleep, the spontaneous drift of the activity packet was similar to that observed during waking and accelerated tenfold during slow-wave sleep.These findings demonstrate that peripheral inputs impinge on an internally organized network, which provides amplification and enhanced precision of the HD signal.

View Article: PubMed Central - PubMed

Affiliation: The Neuroscience Institute, School of Medicine and Center for Neural Science, New York University, New York, New York, USA.

ABSTRACT
The head-direction (HD) system functions as a compass, with member neurons robustly increasing their firing rates when the animal's head points in a specific direction. HD neurons may be driven by peripheral sensors or, as computational models postulate, internally generated (attractor) mechanisms. We addressed the contributions of stimulus-driven and internally generated activity by recording ensembles of HD neurons in the antero-dorsal thalamic nucleus and the post-subiculum of mice by comparing their activity in various brain states. The temporal correlation structure of HD neurons was preserved during sleep, characterized by a 60°-wide correlated neuronal firing (activity packet), both within and across these two brain structures. During rapid eye movement sleep, the spontaneous drift of the activity packet was similar to that observed during waking and accelerated tenfold during slow-wave sleep. These findings demonstrate that peripheral inputs impinge on an internally organized network, which provides amplification and enhanced precision of the HD signal.

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Fast synchronous oscillations in ADn HD cellsa: Bottom, HD fields of the reference cell (dashed curve) and three other HD cells recorded on a different shank. Top: Examples of spike cross-correlogram between the three ADn cell pairs and their normalized (equal to 1 when independent) and z-scored cross-correlograms (number of s.d. from baseline obtained from 100 correlograms of spike trains jittered uniformly in ±10ms windows). Middle, wavelet transforms of z-scored cross-correlograms, all normalized to the same scale. b: Amplitude of pairwise synchrony (in z-values from baseline ± s.e.m., as in panel a) as a function of preferred direction difference (p < 10–10). c: Average power (± s.e.m.) of wavelet-transformed z-scored cross-correlograms across brain states.
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Figure 6: Fast synchronous oscillations in ADn HD cellsa: Bottom, HD fields of the reference cell (dashed curve) and three other HD cells recorded on a different shank. Top: Examples of spike cross-correlogram between the three ADn cell pairs and their normalized (equal to 1 when independent) and z-scored cross-correlograms (number of s.d. from baseline obtained from 100 correlograms of spike trains jittered uniformly in ±10ms windows). Middle, wavelet transforms of z-scored cross-correlograms, all normalized to the same scale. b: Amplitude of pairwise synchrony (in z-values from baseline ± s.e.m., as in panel a) as a function of preferred direction difference (p < 10–10). c: Average power (± s.e.m.) of wavelet-transformed z-scored cross-correlograms across brain states.

Mentions: Finally, we examined the fine timescale dynamics of HD neurons within and across structures. Spectral analysis of cross-correlation functions between pairs of HD cells in the ADn revealed strong oscillatory spiking dynamics activity in windows of approximately 1–5 ms (Fig. 6a). The degree of synchrony decreased with the magnitude of difference between the preferred head directions of the neurons (Fig. 6b; p < 10–10; Kruskal-Wallis test, n = 970 ADn HD cell pairs) in all brain states (Fig. 6c and Supplementary Fig. 7a). The high degree of synchrony displayed by ADn neurons can contribute to the effective discharge of their target neurons in PoS. In support of this hypothesis, cross-correlation analyses between pairs of ADn-PoS neurons revealed putative synaptic connections in a fraction of the pairs (4.45% of 6960 pairs from ADn to PoS, 0.35% from PoS to ADn; see Methods, Fig. 7a,b, Supplementary Fig. 7b), which included both putative PoS pyramidal cells and interneurons (Fig. 7a, Supplementary Fig. 6). When only ADn and PoS pyramidal cell pairs were considered (3394 pairs), we found putative synaptic connections in both directions (Supplementary Fig. 7b) but the probability of feed-forward connections from the ADn to the PoS was twice as high as the PoS to ADn feedback direction (0.41% ADn-PoS pairs versus 0.18% PoS-ADn pairs; p = 0.014, binomial test). ADn cell spiking was associated with high frequency LFP oscillations in the PoS (Fig. 7c), indicating that the fast synchronous oscillation of ADn assemblies was also transmitted to PoS. Furthermore, PoS HD cells that were post-synaptic to ADn HD cells shared the same preferred direction as their presynaptic neuron (Fig. 7d, p = 0.68, Rayleigh test followed by Wilcoxon’s signed rank test, n = 12), suggesting direct forwarding of a ‘copy’ of the thalamic HD signal. Pyramidal neurons in PoS that were synaptically driven by ADn HD cells conveyed more HD information than PoS neurons for which a presynaptic cell could not be identified (Fig. 7e; p = 0.011, Mann-Whitney U-test). No such difference in HD information was observed between ADn neurons and putative interneurons in PoS (Fig. 7e; p = 0.38). These findings demonstrate that ADn and PoS cell assemblies are strongly synchronized and establish effective reciprocal communication.


Internally organized mechanisms of the head direction sense.

Peyrache A, Lacroix MM, Petersen PC, Buzsáki G - Nat. Neurosci. (2015)

Fast synchronous oscillations in ADn HD cellsa: Bottom, HD fields of the reference cell (dashed curve) and three other HD cells recorded on a different shank. Top: Examples of spike cross-correlogram between the three ADn cell pairs and their normalized (equal to 1 when independent) and z-scored cross-correlograms (number of s.d. from baseline obtained from 100 correlograms of spike trains jittered uniformly in ±10ms windows). Middle, wavelet transforms of z-scored cross-correlograms, all normalized to the same scale. b: Amplitude of pairwise synchrony (in z-values from baseline ± s.e.m., as in panel a) as a function of preferred direction difference (p < 10–10). c: Average power (± s.e.m.) of wavelet-transformed z-scored cross-correlograms across brain states.
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Figure 6: Fast synchronous oscillations in ADn HD cellsa: Bottom, HD fields of the reference cell (dashed curve) and three other HD cells recorded on a different shank. Top: Examples of spike cross-correlogram between the three ADn cell pairs and their normalized (equal to 1 when independent) and z-scored cross-correlograms (number of s.d. from baseline obtained from 100 correlograms of spike trains jittered uniformly in ±10ms windows). Middle, wavelet transforms of z-scored cross-correlograms, all normalized to the same scale. b: Amplitude of pairwise synchrony (in z-values from baseline ± s.e.m., as in panel a) as a function of preferred direction difference (p < 10–10). c: Average power (± s.e.m.) of wavelet-transformed z-scored cross-correlograms across brain states.
Mentions: Finally, we examined the fine timescale dynamics of HD neurons within and across structures. Spectral analysis of cross-correlation functions between pairs of HD cells in the ADn revealed strong oscillatory spiking dynamics activity in windows of approximately 1–5 ms (Fig. 6a). The degree of synchrony decreased with the magnitude of difference between the preferred head directions of the neurons (Fig. 6b; p < 10–10; Kruskal-Wallis test, n = 970 ADn HD cell pairs) in all brain states (Fig. 6c and Supplementary Fig. 7a). The high degree of synchrony displayed by ADn neurons can contribute to the effective discharge of their target neurons in PoS. In support of this hypothesis, cross-correlation analyses between pairs of ADn-PoS neurons revealed putative synaptic connections in a fraction of the pairs (4.45% of 6960 pairs from ADn to PoS, 0.35% from PoS to ADn; see Methods, Fig. 7a,b, Supplementary Fig. 7b), which included both putative PoS pyramidal cells and interneurons (Fig. 7a, Supplementary Fig. 6). When only ADn and PoS pyramidal cell pairs were considered (3394 pairs), we found putative synaptic connections in both directions (Supplementary Fig. 7b) but the probability of feed-forward connections from the ADn to the PoS was twice as high as the PoS to ADn feedback direction (0.41% ADn-PoS pairs versus 0.18% PoS-ADn pairs; p = 0.014, binomial test). ADn cell spiking was associated with high frequency LFP oscillations in the PoS (Fig. 7c), indicating that the fast synchronous oscillation of ADn assemblies was also transmitted to PoS. Furthermore, PoS HD cells that were post-synaptic to ADn HD cells shared the same preferred direction as their presynaptic neuron (Fig. 7d, p = 0.68, Rayleigh test followed by Wilcoxon’s signed rank test, n = 12), suggesting direct forwarding of a ‘copy’ of the thalamic HD signal. Pyramidal neurons in PoS that were synaptically driven by ADn HD cells conveyed more HD information than PoS neurons for which a presynaptic cell could not be identified (Fig. 7e; p = 0.011, Mann-Whitney U-test). No such difference in HD information was observed between ADn neurons and putative interneurons in PoS (Fig. 7e; p = 0.38). These findings demonstrate that ADn and PoS cell assemblies are strongly synchronized and establish effective reciprocal communication.

Bottom Line: The temporal correlation structure of HD neurons was preserved during sleep, characterized by a 60°-wide correlated neuronal firing (activity packet), both within and across these two brain structures.During rapid eye movement sleep, the spontaneous drift of the activity packet was similar to that observed during waking and accelerated tenfold during slow-wave sleep.These findings demonstrate that peripheral inputs impinge on an internally organized network, which provides amplification and enhanced precision of the HD signal.

View Article: PubMed Central - PubMed

Affiliation: The Neuroscience Institute, School of Medicine and Center for Neural Science, New York University, New York, New York, USA.

ABSTRACT
The head-direction (HD) system functions as a compass, with member neurons robustly increasing their firing rates when the animal's head points in a specific direction. HD neurons may be driven by peripheral sensors or, as computational models postulate, internally generated (attractor) mechanisms. We addressed the contributions of stimulus-driven and internally generated activity by recording ensembles of HD neurons in the antero-dorsal thalamic nucleus and the post-subiculum of mice by comparing their activity in various brain states. The temporal correlation structure of HD neurons was preserved during sleep, characterized by a 60°-wide correlated neuronal firing (activity packet), both within and across these two brain structures. During rapid eye movement sleep, the spontaneous drift of the activity packet was similar to that observed during waking and accelerated tenfold during slow-wave sleep. These findings demonstrate that peripheral inputs impinge on an internally organized network, which provides amplification and enhanced precision of the HD signal.

Show MeSH