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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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Persistence of information content during wake and sleep in the thalamo-cortical HD circuita: Dual site recording of cell ensembles in the Antero-Dorsal nucleus of the thalamus (ADn) and the post-subiculum (PoS). 4′,6-Diamidino-2-Phenylindole (DAPI) staining of a coronal section through the PoS (top; arrowheads indicate tracks) and ADn (bottom; DAPI combined with parvalbumin yellow fluorescent protein, PV-YFP). RT, reticular nucleus. b: Tuning curves of simultaneously recorded HD cells in the ADn and the PoS. Polar plots indicate average firing rates as a function of the animals’ HD. Colors code for peak firing rate. Middle panel displays average tuning curves (± s.d.) in Cartesian coordinates. c: Activity of HD cell ensembles during wake, SWS and REM sleep. Top: PoS LFP spectrograms; middle: actual (dashed line) and reconstructed HD signal using Bayesian decoding of ADn (red) or PoS (blue) cells; bottom: raster plots of PoS (blue) and ADn (red) cell spike times. Cells were ordered according to their preferred HD during waking. d: Magnified samples from c. Raster plots of neurons are colored according to their preferred HD during waking. Curves show the reconstructed HD signal from ADn HD cells. Circular y-values are shifted for the sake of visibility but color indicates true decoded HD information.
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Figure 1: Persistence of information content during wake and sleep in the thalamo-cortical HD circuita: Dual site recording of cell ensembles in the Antero-Dorsal nucleus of the thalamus (ADn) and the post-subiculum (PoS). 4′,6-Diamidino-2-Phenylindole (DAPI) staining of a coronal section through the PoS (top; arrowheads indicate tracks) and ADn (bottom; DAPI combined with parvalbumin yellow fluorescent protein, PV-YFP). RT, reticular nucleus. b: Tuning curves of simultaneously recorded HD cells in the ADn and the PoS. Polar plots indicate average firing rates as a function of the animals’ HD. Colors code for peak firing rate. Middle panel displays average tuning curves (± s.d.) in Cartesian coordinates. c: Activity of HD cell ensembles during wake, SWS and REM sleep. Top: PoS LFP spectrograms; middle: actual (dashed line) and reconstructed HD signal using Bayesian decoding of ADn (red) or PoS (blue) cells; bottom: raster plots of PoS (blue) and ADn (red) cell spike times. Cells were ordered according to their preferred HD during waking. d: Magnified samples from c. Raster plots of neurons are colored according to their preferred HD during waking. Curves show the reconstructed HD signal from ADn HD cells. Circular y-values are shifted for the sake of visibility but color indicates true decoded HD information.

Mentions: Ensembles of HD neurons from ADn (8.4 ± 5.1 s.d. units per session) and PoS (5 ± 2.8 s.d.) were recorded by multi-site silicon probes (Fig. 1a, Supplementary Fig. 1) in 7 mice foraging for food in an open environment (42 sessions) and in their home cages during sleep (Supplementary Table 1). In 3 mice (21 sessions) ADn and PoS recordings were performed simultaneously. HD cell ensembles covered the full span of head-directions (Fig. 1b–d). ADn and HD cells were characterized by a uniform bell-shaped tuning curve (Fig. 1b; Supplementary Fig. 2a). ADn neurons exhibited peak rates almost three times higher than PoS cells (Supplementary Fig. 2b; p < 10–10, Mann-Whitney U-test, n = 242 ADn and n = 111 PoS HD cells) and conveyed 30% more head-direction information than PoS cells (1.44 bit per spike vs. 1.11 bit per spike; see Methods; Supplementary Fig. 2c; p < 10–6, Mann-Whitney U-test), firing more consistently with the head-direction.


Internally organized mechanisms of the head direction sense.

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

Persistence of information content during wake and sleep in the thalamo-cortical HD circuita: Dual site recording of cell ensembles in the Antero-Dorsal nucleus of the thalamus (ADn) and the post-subiculum (PoS). 4′,6-Diamidino-2-Phenylindole (DAPI) staining of a coronal section through the PoS (top; arrowheads indicate tracks) and ADn (bottom; DAPI combined with parvalbumin yellow fluorescent protein, PV-YFP). RT, reticular nucleus. b: Tuning curves of simultaneously recorded HD cells in the ADn and the PoS. Polar plots indicate average firing rates as a function of the animals’ HD. Colors code for peak firing rate. Middle panel displays average tuning curves (± s.d.) in Cartesian coordinates. c: Activity of HD cell ensembles during wake, SWS and REM sleep. Top: PoS LFP spectrograms; middle: actual (dashed line) and reconstructed HD signal using Bayesian decoding of ADn (red) or PoS (blue) cells; bottom: raster plots of PoS (blue) and ADn (red) cell spike times. Cells were ordered according to their preferred HD during waking. d: Magnified samples from c. Raster plots of neurons are colored according to their preferred HD during waking. Curves show the reconstructed HD signal from ADn HD cells. Circular y-values are shifted for the sake of visibility but color indicates true decoded HD information.
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Figure 1: Persistence of information content during wake and sleep in the thalamo-cortical HD circuita: Dual site recording of cell ensembles in the Antero-Dorsal nucleus of the thalamus (ADn) and the post-subiculum (PoS). 4′,6-Diamidino-2-Phenylindole (DAPI) staining of a coronal section through the PoS (top; arrowheads indicate tracks) and ADn (bottom; DAPI combined with parvalbumin yellow fluorescent protein, PV-YFP). RT, reticular nucleus. b: Tuning curves of simultaneously recorded HD cells in the ADn and the PoS. Polar plots indicate average firing rates as a function of the animals’ HD. Colors code for peak firing rate. Middle panel displays average tuning curves (± s.d.) in Cartesian coordinates. c: Activity of HD cell ensembles during wake, SWS and REM sleep. Top: PoS LFP spectrograms; middle: actual (dashed line) and reconstructed HD signal using Bayesian decoding of ADn (red) or PoS (blue) cells; bottom: raster plots of PoS (blue) and ADn (red) cell spike times. Cells were ordered according to their preferred HD during waking. d: Magnified samples from c. Raster plots of neurons are colored according to their preferred HD during waking. Curves show the reconstructed HD signal from ADn HD cells. Circular y-values are shifted for the sake of visibility but color indicates true decoded HD information.
Mentions: Ensembles of HD neurons from ADn (8.4 ± 5.1 s.d. units per session) and PoS (5 ± 2.8 s.d.) were recorded by multi-site silicon probes (Fig. 1a, Supplementary Fig. 1) in 7 mice foraging for food in an open environment (42 sessions) and in their home cages during sleep (Supplementary Table 1). In 3 mice (21 sessions) ADn and PoS recordings were performed simultaneously. HD cell ensembles covered the full span of head-directions (Fig. 1b–d). ADn and HD cells were characterized by a uniform bell-shaped tuning curve (Fig. 1b; Supplementary Fig. 2a). ADn neurons exhibited peak rates almost three times higher than PoS cells (Supplementary Fig. 2b; p < 10–10, Mann-Whitney U-test, n = 242 ADn and n = 111 PoS HD cells) and conveyed 30% more head-direction information than PoS cells (1.44 bit per spike vs. 1.11 bit per spike; see Methods; Supplementary Fig. 2c; p < 10–6, Mann-Whitney U-test), firing more consistently with the head-direction.

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