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Temporal synchrony and gamma-to-theta power conversion in the dendrites of CA1 pyramidal neurons.

Vaidya SP, Johnston D - Nat. Neurosci. (2013)

Bottom Line: Here we show that pyramidal neurons in the rodent hippocampus use a gradient of inductance in the form of hyperpolarization-activated cation-nonselective (HCN) channels as an active mechanism to counteract location-dependent temporal differences of dendritic inputs at the soma.Using simultaneous multi-site whole-cell recordings complemented by computational modeling, we find that this intrinsic biophysical mechanism produces temporal synchrony of rhythmic inputs in the theta and gamma frequency ranges across wide regions of the dendritic tree.While gamma and theta oscillations are known to synchronize activity across space in neuronal networks, our results identify a new mechanism by which this synchrony extends to activity within single pyramidal neurons with complex dendritic arbors.

View Article: PubMed Central - PubMed

Affiliation: 1] Institute for Neuroscience Graduate Program, The University of Texas at Austin, Austin, Texas, USA. [2] Center for Learning and Memory, The University of Texas at Austin, Austin, Texas, USA.

ABSTRACT
Timing is a crucial aspect of synaptic integration. For pyramidal neurons that integrate thousands of synaptic inputs spread across hundreds of microns, it is thus a challenge to maintain the timing of incoming inputs at the axo-somatic integration site. Here we show that pyramidal neurons in the rodent hippocampus use a gradient of inductance in the form of hyperpolarization-activated cation-nonselective (HCN) channels as an active mechanism to counteract location-dependent temporal differences of dendritic inputs at the soma. Using simultaneous multi-site whole-cell recordings complemented by computational modeling, we find that this intrinsic biophysical mechanism produces temporal synchrony of rhythmic inputs in the theta and gamma frequency ranges across wide regions of the dendritic tree. While gamma and theta oscillations are known to synchronize activity across space in neuronal networks, our results identify a new mechanism by which this synchrony extends to activity within single pyramidal neurons with complex dendritic arbors.

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Gamma frequency synaptic bursts generate theta-frequency components important for oscillatory synchrony(a) describes the synaptic current input at 300 μm and the corresponding voltage output at the soma for bursts of increasing frequencies. (b) &(c) depict the frequency components for the current input and voltage output in (a) respectively. Note that all the high frequency components are filtered out and only the slow frequency components make up the voltage waveform at the soma. (d) describes the peak of the low frequency current component in the dendrite which determines the voltage waveform at the soma for increasing burst frequencies from 20 Hz to 180 Hz. Note that the peak component of burst frequencies from 50 – 140 Hz corresponds with the theta frequency range for bursts with 5 synaptic inputs. (e) Same as (d) but with the number of impulses per burst changing from 2–10 (f) represents the impedance measured at the peak slow frequency component for increasing burst frequency. (gray) lines represent individual cells while red solid line represents the average and s.e.m for the 4 cells. Note that the maximum impedance is for gamma frequency bursts as would be predicted from (d). Error bars indicate s.e.m.
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Figure 7: Gamma frequency synaptic bursts generate theta-frequency components important for oscillatory synchrony(a) describes the synaptic current input at 300 μm and the corresponding voltage output at the soma for bursts of increasing frequencies. (b) &(c) depict the frequency components for the current input and voltage output in (a) respectively. Note that all the high frequency components are filtered out and only the slow frequency components make up the voltage waveform at the soma. (d) describes the peak of the low frequency current component in the dendrite which determines the voltage waveform at the soma for increasing burst frequencies from 20 Hz to 180 Hz. Note that the peak component of burst frequencies from 50 – 140 Hz corresponds with the theta frequency range for bursts with 5 synaptic inputs. (e) Same as (d) but with the number of impulses per burst changing from 2–10 (f) represents the impedance measured at the peak slow frequency component for increasing burst frequency. (gray) lines represent individual cells while red solid line represents the average and s.e.m for the 4 cells. Note that the maximum impedance is for gamma frequency bursts as would be predicted from (d). Error bars indicate s.e.m.

Mentions: To identify the temporal patterns of synaptic inputs that maximize oscillatory synchrony, we started with the burst input and altered the frequency of the synaptic events within the burst (Fig. 7a). We then analyzed the slow-frequency components in the dendritic current input that constitute the majority of the voltage output at the soma (Fig. 7b, c). Our results show that burst frequencies in the gamma frequency range (40–140 Hz) generate a slow input current component that peaks in the theta frequency range (4–10 Hz) (Fig. 7d). Additional experiments suggest that this relationship, though dependent on the burst size, holds true for synaptic bursts consisting of 3–9 impulses (Fig. 7e). Assuming gamma bursts occur on either the peak or valley of a 7 Hz theta cycle32, this range of impulses per synaptic burst would be relevant for the entire range of gamma frequencies between 40 and 120 Hz.


Temporal synchrony and gamma-to-theta power conversion in the dendrites of CA1 pyramidal neurons.

Vaidya SP, Johnston D - Nat. Neurosci. (2013)

Gamma frequency synaptic bursts generate theta-frequency components important for oscillatory synchrony(a) describes the synaptic current input at 300 μm and the corresponding voltage output at the soma for bursts of increasing frequencies. (b) &(c) depict the frequency components for the current input and voltage output in (a) respectively. Note that all the high frequency components are filtered out and only the slow frequency components make up the voltage waveform at the soma. (d) describes the peak of the low frequency current component in the dendrite which determines the voltage waveform at the soma for increasing burst frequencies from 20 Hz to 180 Hz. Note that the peak component of burst frequencies from 50 – 140 Hz corresponds with the theta frequency range for bursts with 5 synaptic inputs. (e) Same as (d) but with the number of impulses per burst changing from 2–10 (f) represents the impedance measured at the peak slow frequency component for increasing burst frequency. (gray) lines represent individual cells while red solid line represents the average and s.e.m for the 4 cells. Note that the maximum impedance is for gamma frequency bursts as would be predicted from (d). Error bars indicate s.e.m.
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Related In: Results  -  Collection

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Figure 7: Gamma frequency synaptic bursts generate theta-frequency components important for oscillatory synchrony(a) describes the synaptic current input at 300 μm and the corresponding voltage output at the soma for bursts of increasing frequencies. (b) &(c) depict the frequency components for the current input and voltage output in (a) respectively. Note that all the high frequency components are filtered out and only the slow frequency components make up the voltage waveform at the soma. (d) describes the peak of the low frequency current component in the dendrite which determines the voltage waveform at the soma for increasing burst frequencies from 20 Hz to 180 Hz. Note that the peak component of burst frequencies from 50 – 140 Hz corresponds with the theta frequency range for bursts with 5 synaptic inputs. (e) Same as (d) but with the number of impulses per burst changing from 2–10 (f) represents the impedance measured at the peak slow frequency component for increasing burst frequency. (gray) lines represent individual cells while red solid line represents the average and s.e.m for the 4 cells. Note that the maximum impedance is for gamma frequency bursts as would be predicted from (d). Error bars indicate s.e.m.
Mentions: To identify the temporal patterns of synaptic inputs that maximize oscillatory synchrony, we started with the burst input and altered the frequency of the synaptic events within the burst (Fig. 7a). We then analyzed the slow-frequency components in the dendritic current input that constitute the majority of the voltage output at the soma (Fig. 7b, c). Our results show that burst frequencies in the gamma frequency range (40–140 Hz) generate a slow input current component that peaks in the theta frequency range (4–10 Hz) (Fig. 7d). Additional experiments suggest that this relationship, though dependent on the burst size, holds true for synaptic bursts consisting of 3–9 impulses (Fig. 7e). Assuming gamma bursts occur on either the peak or valley of a 7 Hz theta cycle32, this range of impulses per synaptic burst would be relevant for the entire range of gamma frequencies between 40 and 120 Hz.

Bottom Line: Here we show that pyramidal neurons in the rodent hippocampus use a gradient of inductance in the form of hyperpolarization-activated cation-nonselective (HCN) channels as an active mechanism to counteract location-dependent temporal differences of dendritic inputs at the soma.Using simultaneous multi-site whole-cell recordings complemented by computational modeling, we find that this intrinsic biophysical mechanism produces temporal synchrony of rhythmic inputs in the theta and gamma frequency ranges across wide regions of the dendritic tree.While gamma and theta oscillations are known to synchronize activity across space in neuronal networks, our results identify a new mechanism by which this synchrony extends to activity within single pyramidal neurons with complex dendritic arbors.

View Article: PubMed Central - PubMed

Affiliation: 1] Institute for Neuroscience Graduate Program, The University of Texas at Austin, Austin, Texas, USA. [2] Center for Learning and Memory, The University of Texas at Austin, Austin, Texas, USA.

ABSTRACT
Timing is a crucial aspect of synaptic integration. For pyramidal neurons that integrate thousands of synaptic inputs spread across hundreds of microns, it is thus a challenge to maintain the timing of incoming inputs at the axo-somatic integration site. Here we show that pyramidal neurons in the rodent hippocampus use a gradient of inductance in the form of hyperpolarization-activated cation-nonselective (HCN) channels as an active mechanism to counteract location-dependent temporal differences of dendritic inputs at the soma. Using simultaneous multi-site whole-cell recordings complemented by computational modeling, we find that this intrinsic biophysical mechanism produces temporal synchrony of rhythmic inputs in the theta and gamma frequency ranges across wide regions of the dendritic tree. While gamma and theta oscillations are known to synchronize activity across space in neuronal networks, our results identify a new mechanism by which this synchrony extends to activity within single pyramidal neurons with complex dendritic arbors.

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