scholarly journals Physiological noise optimizes multiplexed coding of vibrotactile-like signals in somatosensory cortex

2021 ◽  
Author(s):  
Mohammad Amin Kamaleddin ◽  
Aaron Shifman ◽  
Daniel MW Sigal ◽  
Steven A Prescott

ABSTRACTNeurons can use different aspects of their spiking to simultaneously represent (multiplex) different features of a stimulus. For example, some pyramidal neurons in primary somatosensory cortex (S1) use the rate and timing of their spikes to respectively encode the intensity and frequency of vibrotactile stimuli. Doing so has several requirements. Because they fire at low rates, pyramidal neurons cannot entrain 1:1 with high-frequency (100-600 Hz) inputs and instead must skip (i.e. not respond to) some stimulus cycles. The proportion of skipped cycles must vary inversely with stimulus intensity for firing rate to encode stimulus intensity. Spikes must phase lock to the stimulus for spike times (intervals) to encode stimulus frequency but, in addition, skipping must occur irregularly to avoid aliasing. Using simulations and in vitro experiments in which S1 pyramidal neurons were stimulated with inputs emulating those induced by vibrotactile stimuli, we show that fewer cycles are skipped as stimulus intensity increases, as required for rate coding, and that physiological noise induces irregular skipping without disrupting phase locking, as required for temporal coding. This occurs because the reliability and precision of spikes evoked by small- amplitude, fast-onset signals are differentially sensitive to noise. Simulations confirmed that differences in stimulus intensity and frequency can be well discriminated based on differences in spike rate or timing, respectively, but only in the presence of noise. Our results show that multiplexed coding by S1 pyramidal neurons is facilitated rather than degraded by physiological levels of noise. In fact, multiplexing is optimal under physiologically noisy conditions.

2008 ◽  
Vol 99 (3) ◽  
pp. 1394-1407 ◽  
Author(s):  
Sarah Potez ◽  
Matthew E. Larkum

Understanding the impact of active dendritic properties on network activity in vivo has so far been restricted to studies in anesthetized animals. However, to date no study has been made to determine the direct effect of the anesthetics themselves on dendritic properties. Here, we investigated the effects of three types of anesthetics commonly used for animal experiments (urethane, pentobarbital and ketamine/xylazine). We investigated the generation of calcium spikes, the propagation of action potentials (APs) along the apical dendrite and the somatic firing properties in the presence of anesthetics in vitro using dual somatodendritic whole cell recordings. Calcium spikes were evoked with dendritic current injection and high-frequency trains of APs at the soma. Surprisingly, we found that the direct actions of anesthetics on calcium spikes were very different. Two anesthetics (urethane and pentobarbital) suppressed dendritic calcium spikes in vitro, whereas a mixture of ketamine and xylazine enhanced them. Propagation of spikes along the dendrite was not significantly affected by any of the anesthetics but there were various changes in somatic firing properties that were highly dependent on the anesthetic. Last, we examined the effects of anesthetics on calcium spike initiation and duration in vivo using high-frequency trains of APs generated at the cell body. We found the same anesthetic-dependent direct effects in addition to an overall reduction in dendritic excitability in anesthetized rats with all three anesthetics compared with the slice preparation.


Science ◽  
1986 ◽  
Vol 232 (4746) ◽  
pp. 85-87 ◽  
Author(s):  
Kelso ◽  
TH Brown

An electrophysiological stimulation paradigm similar to one that produces Pavlovian conditioning was applied to synaptic inputs to pyramidal neurons of hippocampal brain slices. Persistent synaptic enhancement was induced in one of two weak synaptic inputs by pairing high-frequency electrical stimulation of the weak input with stimulation of a third, stronger input to the same region. Forward (temporally overlapping) but not backward (temporally separate) pairings caused this enhancement. Thus hippocampal synapses in vitro can undergo the conditional and selective type of associative modification that could provide the substrate for some of the mnemonic functions in which the hippocampus is thought to participate.


2021 ◽  
Author(s):  
Benjamin M. Zemel ◽  
Alexander A. Nevue ◽  
Andre Dagostin ◽  
Peter V. Lovell ◽  
Claudio V. Mello ◽  
...  

AbstractThe underlying mechanisms that promote precise spiking in upper motor neurons controlling fine motor skills are not well understood. Here we report that projection neurons in the adult zebra finch song nucleus RA display: 1) robust high-frequency firing, 2) ultra-short half-width spike waveforms, 3) superfast Na+ current inactivation kinetics and 4) large resurgent Na+ currents (INaR). These spiking properties closely resemble those of specialized pyramidal neurons in mammalian motor cortex and are well suited for precise temporal coding. They emerge during the critical period for vocal learning in males but not females, coinciding with a complete switch of modulatory Na+ channel subunit expression from Navβ3 to Navβ4. Dynamic clamping and dialysis of Navβ4’s C-terminal peptide into juvenile RA neurons provide evidence that this subunit, and its associated INaR, promote neuronal excitability. We propose that Navβ4 underpins INaR that facilitates precise, prolonged, and reliable high-frequency firing in upper motor neurons.


1996 ◽  
Vol 76 (6) ◽  
pp. 4180-4184 ◽  
Author(s):  
D. Plenz ◽  
S. T. Kitai

1. Rhythmic cortical activity was investigated with intracellular recordings in cortex-striatum-mesencephalon organotypic cultures grown for 42 +/- 3 (SE) days in vitro. 2. Electrical stimulation of supragranular layers induced a self-sustained high-frequency oscillation (HFO) in pyramidal neurons and interneurons. 3. The HFO started 197 +/- 39 ms after stimulation and had a mean duration of 1.0 +/- 0.2 s and an initial frequency of 38 +/- 2 Hz. A decrease in frequency at a rate of 11.5 +/- 2.7 Hz/s started on average 547 +/- 109 ms after the onset of the HFO. 4. During the HFO, local interneurons and pyramidal neurons synchronized their activities. The synaptic origin of the HFO was confirmed by its reversal potential at -57 +/- 4 mV. 5. These results suggest that a self-maintained HFO can be induced in local cortical circuits by excitation of supragranular layers. This HFO would facilitate synchronization between distant cortical and thalamic regions.


Author(s):  
Javier Nogueira ◽  
María E. Castelló ◽  
Carolina Lescano ◽  
Ángel A. Caputi

Early sensory relays circuits in the vertebrate medulla often adopt a cerebellum-like organization specialized for comparing primary afferent inputs with central expectations. These circuits usually have a dual output, carried by center ON and center OFF neurons responding in opposite ways to the same stimulus at the center of their receptive fields. Here we show in the electrosensory lateral line lobe of Gymnotiform weakly electric fish that basilar pyramidal neurons, representing ‘ON’ cells, and non-basilar pyramidal neurons, representing ‘OFF’ cells, have different intrinsic electrophysiological properties. We used classical anatomical techniques and electrophysiological in vitro recordings to compare these neurons. Basilar neurons are silent at rest, have a high threshold to intracellular stimulation, delayed responses to steady state depolarization and low pass responsiveness to membrane voltage variations. They respond to low intensity depolarizing stimuli with large, isolated spikes. As stimulus intensity increases the spikes are followed by a depolarizing after-potential from which phase-locked spikes often arise. Non-basilar neurons show a pacemaker-like spiking activity, smoothly modulated in frequency by slow variations of stimulus intensity. Spike frequency adaptation provides a memory of their recent firing, facilitating non-basilar response to stimulus transients. Considering anatomical and functional dimensions we conclude that basilar and non-basilar pyramidal neurons are clear-cut, different anatomo-functional phenotypes. We propose that, in addition to their role in contrast processing, basilar pyramidal neurons encode sustained global stimuli as those elicited by large or distant objects while non-basilar pyramidal neurons respond to transient stimuli due to movement textured nearby objects.


2016 ◽  
Vol 113 (30) ◽  
pp. E4304-E4310 ◽  
Author(s):  
Rebecca L. Warren ◽  
Sripriya Ramamoorthy ◽  
Nikola Ciganović ◽  
Yuan Zhang ◽  
Teresa M. Wilson ◽  
...  

Low-frequency hearing is critically important for speech and music perception, but no mechanical measurements have previously been available from inner ears with intact low-frequency parts. These regions of the cochlea may function in ways different from the extensively studied high-frequency regions, where the sensory outer hair cells produce force that greatly increases the sound-evoked vibrations of the basilar membrane. We used laser interferometry in vitro and optical coherence tomography in vivo to study the low-frequency part of the guinea pig cochlea, and found that sound stimulation caused motion of a minimal portion of the basilar membrane. Outside the region of peak movement, an exponential decline in motion amplitude occurred across the basilar membrane. The moving region had different dependence on stimulus frequency than the vibrations measured near the mechanosensitive stereocilia. This behavior differs substantially from the behavior found in the extensively studied high-frequency regions of the cochlea.


2005 ◽  
Vol 94 (1) ◽  
pp. 501-511 ◽  
Author(s):  
Peter W. Hickmott

Peripheral denervation causes significant changes in the organization of developing or adult primary somatosensory cortex (S1). However, the basic mechanisms that underlie reorganization are not well understood. Most attention has been focused on possible synaptic mechanisms associated with reorganization. However, another important determinant of cortical circuit function is the intrinsic membrane properties of neurons in the circuit. Here we document changes in the intrinsic properties of pyramidal neurons in cortical layer 2/3 in adult rat primary somatosensory cortex (S1) after varying durations of forepaw denervation. Denervation of the forepaw induced a rapid and sustained shift in the location of the border between the forepaw and lower jaw representations of adult S1 (reorganization). Coronal slices from the reorganized region were maintained in vitro and the intrinsic properties of layer 2/3 pyramidal neurons of S1 were determined using whole cell recordings. In general, passive membrane properties were not affected by denervation; however, a variety of active properties were. The most robust changes were increases in the amplitudes of the fast and medium afterhyperpolarization (AHP) and an increase in the interval between action potentials (APs). Additional changes at some durations of denervation were observed for the AP threshold. These observations indicate that changes in intrinsic properties, mostly reflecting a decrease in overall excitation, may play a role in changes in cortical circuit properties during reorganization in adult S1, and suggest a possible role for AHPs in some of those changes.


2004 ◽  
Vol 92 (2) ◽  
pp. 939-948 ◽  
Author(s):  
G. Marsat ◽  
G. S. Pollack

The omega neuron 1 (ON1) of the cricket Teleogryllus oceanicus responds to conspecific signals (4.5 kHz) and to the ultrasonic echolocation sounds used by hunting, insectivorous bats. These signals differ in temporal structure as well as in carrier frequency. We show that ON1's temporal coding properties vary with carrier frequency, allowing it to encode both of these behaviorally important signals. Information-transfer functions show that coding of 4.5 kHz is limited to the range of amplitude-modulation components that occur in cricket songs (<32 Hz), whereas coding of 30-kHz stimuli extends to the higher pulse rates that occur in bat sounds (∼100 Hz). Nonlinear coding contributes to the information content of ON1's spike train, particularly for 30-kHz stimuli with high intensities and large modulation depths. Phase locking to sinusoidal amplitude envelopes also extends to higher AM frequencies for ultrasound stimuli. ON1s frequency-specific behavior cannot be ascribed to differences in the shapes of information-transfer functions of low- and high-frequency-tuned receptor neurons, both of which are tuned more broadly to AM frequencies than ON1. Coding properties are nearly unaffected by contralateral deafferentation. ON1's role in auditory processing is to increase binaural contrast through contralateral inhibition. We hypothesize that its frequency-specific temporal coding properties optimize binaural contrast for sounds with both the spectral and temporal features of behaviorally relevant signals.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
L. Godenzini ◽  
D. Alwis ◽  
R. Guzulaitis ◽  
S. Honnuraiah ◽  
G. J. Stuart ◽  
...  

AbstractThe capacity of the brain to encode multiple types of sensory input is key to survival. Yet, how neurons integrate information from multiple sensory pathways and to what extent this influences behavior is largely unknown. Using two-photon Ca2+ imaging, optogenetics and electrophysiology in vivo and in vitro, we report the influence of auditory input on sensory encoding in the somatosensory cortex and show its impact on goal-directed behavior. Monosynaptic input from the auditory cortex enhanced dendritic and somatic encoding of tactile stimulation in layer 2/3 (L2/3), but not layer 5 (L5), pyramidal neurons in forepaw somatosensory cortex (S1). During a tactile-based goal-directed task, auditory input increased dendritic activity and reduced reaction time, which was abolished by photoinhibition of auditory cortex projections to forepaw S1. Taken together, these results indicate that dendrites of L2/3 pyramidal neurons encode multisensory information, leading to enhanced neuronal output and reduced response latency during goal-directed behavior.


Sign in / Sign up

Export Citation Format

Share Document