Layers Of Barrel Cortex Research Articles

Inter and intralaminar excitation of parvalbumin interneurons in mouse barrel cortex.

Parvalbumin (PV) interneurons are inhibitory fast-spiking cells with essential roles in directing the flow of information through cortical circuits. These neurons set the balance between excitation and inhibition and control rhythmic activity. PV interneurons differ between cortical layers in their morphology, circuitry, and function, but how their electrophysiological properties vary has received little attention. Here we investigate responses of PV interneurons in different layers of primary somatosensory barrel cortex (BC) to different excitatory inputs. With the genetically-encoded hybrid voltage sensor, hVOS, we recorded voltage changes in many L2/3 and L4 PV interneurons simultaneously, with stimulation applied to either L2/3 or L4. A semi-automated procedure was developed to identify small regions of interest corresponding to single responsive PV interneurons. Amplitude, half-width, and rise-time were greater for PV interneurons residing in L2/3 compared to L4. Stimulation in L2/3 elicited responses in both L2/3 and L4 with longer latency compared to stimulation in L4. These differences in latency between layers could influence their windows for temporal integration. Thus, PV interneurons in different cortical layers of BC respond in a layer specific and input specific manner, and these differences have potential roles in cortical computations.

Developmental Phase Transitions in Spatial Organization of Spontaneous Activity in Postnatal Barrel Cortex Layer 4.

Spatially-organized spontaneous activity is a characteristic feature of developing mammalian sensory systems. However, the transitions of spontaneous-activity spatial organization during development and related mechanisms remain largely unknown. We reported previously that layer 4 (L4) glutamatergic neurons in the mouse barrel cortex exhibit spontaneous activity with a patchwork-type pattern at postnatal day (P)5, which is during barrel formation. In the current work, we revealed that spontaneous activity in mouse barrel-cortex L4 glutamatergic neurons exhibits at least three phases during the first two weeks of postnatal development. Phase I activity has a patchwork-type pattern and is observed not only at P5, but also P1, before barrel formation. Phase II is found at P9, by which time barrel formation is completed, and exhibits broadly synchronized activity across barrel borders. Phase III emerges around P11 when L4-neuron activity is desynchronized. The Phase I activity, but not Phase II or III activity, is blocked by thalamic inhibition, demonstrating that the Phase I to II transition is associated with loss of thalamic dependency. Dominant-negative (DN)-Rac1 expression in L4 neurons hampers the Phase II to III transition. It also suppresses developmental increases in spine density and excitatory synapses of L4 neurons in the second postnatal week, suggesting that Rac1-mediated synapse maturation could underlie the Phase II to III transition. Our findings revealed the presence of distinct mechanisms for Phase I to II and Phase II to III transition. They also highlighted the role of a small GTPase in the developmental desynchronization of cortical spontaneous activity.SIGNIFICANCE STATEMENT Developing neocortex exhibits spatially-organized spontaneous activity, which plays a critical role in cortical circuit development. The features of spontaneous-activity spatial organization and the mechanisms underlying its changes during development remain largely unknown. In the present study, using two-photon in vivo imaging, we revealed three phases (Phases I, II, and III) of spontaneous activity in barrel-cortex layer 4 (L4) glutamatergic neurons during the first two postnatal weeks. We also demonstrated the presence of distinct mechanisms underlying phase transitions. Phase I to II shift arose from the switch in the L4-neuron driving source, and Phase II to III transition relied on L4-neuron Rac1 activity. These results provide new insights into the principles of developmental transitions of neocortical spontaneous-activity spatial patterns.

Temporal refinement of sensory-evoked activity across layers in developing mouse barrel cortex.

Rhythmic whisking behavior in rodents fully develops during a critical period about 2weeks after birth, in parallel with the maturation of other sensory modalities and the onset of exploratory locomotion. How whisker-related sensory processing develops during this period in the primary somatosensory cortex (S1) remains poorly understood. Here, we characterized neuronal activity evoked by single- or dual-whisker stimulation patterns in developing S1, before, during and after the occurrence of active whisking. Employing multi-electrode recordings in all layers of barrel cortex in urethane-anesthetized mice, we find layer-specific changes in multi-unit activity for principal and neighboring barrel columns. While whisker stimulation evoked similar early responses (0-50ms post-stimulus) across development, the late response (50-150ms post-stimulus) decreased in all layers with age. Furthermore, peak onset times and the duration of the late response decreased in all layers across age groups. Responses to paired-pulse stimulation showed increases in spiking precision and in paired-pulse ratios in all cortical layers during development. Sequential activation of two neighboring whiskers with varying stimulus intervals evoked distinct response profiles in the activated barrel columns, depending on the direction and temporal separation of the stimuli. In conclusion, our findings indicate that the temporal sharpening of sensory-evoked activity coincides with the onset of active whisking.

Interspersed Distribution of Selectivity to Kinematic Stimulus Features in Supragranular Layers of Mouse Barrel Cortex.

Neurons in the primary sensory regions of neocortex have heterogeneous response properties. The spatial arrangement of neurons with particular response properties is a key aspect of population representations and can shed light on how local circuits are wired. Here, we investigated how neurons with sensitivity to different kinematic features of whisker stimuli are distributed across local circuits in supragranular layers of the barrel cortex. Using 2-photon calcium population imaging in anesthetized mice, we found that nearby neurons represent diverse kinematic features, providing a rich population representation at the local scale. Neurons interspersed in space therefore responded differently to a common stimulus kinematic feature. Conversely, neurons with similar feature selectivity were located no closer to each other than predicted by a random distribution null hypothesis. This finding relied on defining a null hypothesis that was specific for testing the spatial distribution of tuning across neurons. We also measured how neurons sensitive to specific features were distributed relative to barrel boundaries, and found no systematic organization. Our results are compatible with randomly distributed selectivity to kinematic features, with no systematic ordering superimposed upon the whisker map.

The Functional Organization of Neocortical Networks Investigated in Slices with Local Field Recordings and Laser Scanning Photostimulation.

The organization of cortical networks can be investigated functionally in brain slices. Laser scanning photostimulation (LSPS) with glutamate-uncaging allows for a rapid survey of all connections impinging on single cells recorded in patch-clamp. We sought to develop a variant of the method that would allow for a more exhaustive mapping of neuronal networks at every experiment. We found that the extracellular field recordings could be used to detect synaptic responses evoked by LSPS. One to two electrodes were placed in all six cortical layers of barrel cortex successively and maps were computed from the size of synaptic negative local field potentials. The field maps displayed a laminar organization similar to the one observed in maps computed from excitatory postsynaptic currents recorded in patch-clamp mode. Thus, LSPS combined with field recording is an interesting alternative to obtain for every animal tested a comprehensive map of the excitatory intracortical network.

Information Processing Streams in Rodent Barrel Cortex: The Differential Functions of Barrel and Septal Circuits

Rodent somatosensory cortex contains an isomorphic map of the mystacial whiskers in which each whisker is represented by neuronal populations, or barrels, that are separated from each other by intervening septa. Separate afferent pathways convey somatosensory information to the barrels and septa that represent the input stages for 2 partially segregated circuits that extend throughout the other layers of barrel cortex. Whereas the barrel-related circuits process spatiotemporal information generated by whisker contact with external objects, the septa-related circuits encode the frequency and other kinetic features of active whisker movements. The projection patterns from barrel cortex indicate that information processed by the septa-related circuits is used both separately and in combination with information from the barrel-related circuits to mediate specific functions. According to this theory, outputs from the septal processing stream modulate the brain regions that regulate whisking behavior, whereas both processing streams cooperate with each other to identify external stimuli encountered by passive or active whisker movements. This theoretical view prompts several testable hypotheses about the coordination of neuronal activity during whisking behavior. Foremost among these, motor brain regions that control whisker movements are more strongly coordinated with the septa-related circuits than with the barrel-related circuits.

Detection psychophysics of intracortical microstimulation in rat primary somatosensory cortex

A problem of purposeful intracortical microstimulation is the long duration of neuronal integration time and the associated complex temporal interactions of effects to individual pulses in trains. Here we investigated the effects of repetitive stimuli on perception. We trained head-restraint rats to indicate the detection of cortical microstimulation in infragranular layers of barrel cortex. Three stimulus parameters: stimulus intensity, number of pulses and frequency were varied, and psychometric detection curves were assessed using the method of constant stimuli. The average psychophysical threshold of single pulses was 2.0 nC--a measure very close to what has been found earlier for the evocation of short-latency action potentials in neurons near the stimulation electrode. Detection of single-pulse stimulation always saturated at probabilities of about 0.8. In contrast, repetitive stimuli gave rise to lower thresholds (by a factor of two at 15 pulses, 320 Hz), and to saturation at probabilities close to 1. Interestingly, a large fraction of these perceptual benefits was observed already with double pulses. Moreover, the perceptual efficacy of individual pulses was higher using double pulses compared with longer sequences, i.e. double pulses were detected better than expected from the assumption of independence of single-pulse effects, while trains of 15 pulses fell well short of this expectation. The present results thus point to double-pulse stimulation as an optimal choice when trading economic stimulation against optimizing of the percept.

Differential origin of projections from SI barrel cortex to the whisker representations in SII and MI

We have previously shown that projections from SI barrel cortex to the MI whisker representation originate primarily from columns of neurons that are aligned with the layer IV septa. SI barrel cortex also projects to SII cortex, but the origin of these projections has not been characterized with respect to the barrel and septal compartments. To address this issue, we injected retrograde tracers into the SII whisker representation and then reconstructed the location of the labeled neurons in SI with respect to the layer IV barrels. In some animals, two different tracers were injected into the whisker representations of SII and MI to detect double-labeled neurons that would indicate that some SI neurons project to both of these cortical areas. We found that the projections to SII cortex originate from sites that are uniformly distributed throughout the extragranular layers of barrel cortex. In cases in which different tracers were injected in SII and MI, double-labeled neurons appeared above and below the layer IV septal compartment and at sites aligned with the boundaries of the layer IV barrels. To the extent that the columns of neurons aligned with the barrel and septal compartments represent functionally distinct circuits, these results indicate that SII receives information from both circuits, whereas MI receives inputs primarily from the septal circuits.

Central Signals Rapidly Switch Tactile Processing in Rat Barrel Cortex during Whisker Movements

Palpatory movements ('active' touch) are an integral part of tactile sensing. It is known that tactile signals can be modulated in certain behavioral contexts, but it is still unresolved to what degree this modulation is related to movement kinematics and whether it stems from tactile receptors or from central sources. Using awake, head-fixed rats, trained to contact an object, we measured trajectories of muscle-propelled whisker movement precisely and compared tactile responses to contacts thus accomplished with 'passive' contacts (motionless whisker contacted by object). Multielectrode extracellular recordings in deep layers of barrel cortex revealed that when the animals moved their whiskers actively, tactile processing switched from high response amplitudes, wide cortical representation and low background firing, to low response amplitudes, narrow spatial representation and elevated background firing. Switching was fast (<100 ms) and unrelated to the degree of alertness as assessed by spectral analysis of pre-contact field potentials. Switching persisted when information about whisker kinematics was interrupted by transection of the infraorbital nerve and contacts were mimicked by peripheral electrical stimulation. Taken together, these characteristics render central signals derived from the motor system a likely contributor to the processing of active touch.

Encoding of Whisker Vibration by Rat Barrel Cortex Neurons: Implications for Texture Discrimination

Rats, using their whiskers, have excellent capabilities in texture discrimination. What is the representation of texture in rat somatosensory cortex? We hypothesize that as rats "whisk" over a surface, the spatial frequency of a grooved or pebbled texture is converted to a temporal frequency of whisker vibration. Surface features such as groove depth or grain size modulate the amplitude of this vibration. Validation of the hypothesis depends on showing that vibration parameters have distinct neuronal representations in cortex. To test this, we delivered sinusoidal vibrations to the whisker shaft and analyzed cortical neuronal activity. Seven amplitudes and seven frequencies were combined to construct 49 stimuli while recording activity through a 10 x 10 microelectrode array inserted into the middle layers of barrel cortex. We find that cortical neurons do not explicitly encode vibration frequency (f) or amplitude (A) by any coding measure (average spike counts over different time windows, spike timing patterns in the peristimulus time histograms or in autocorrelograms). Instead, neurons explicitly encode the product of frequency and amplitude, which is proportional to the mean speed of the vibration. The quantity Af is an invariant because neuronal response encodes this feature independently of the values of the individual terms A and f. This was true across a wide time scale of firing rate measurements, from 5 to 500 msec. We conclude that vibration kinetics are rapidly and reliably encoded in the firing rate of cortical ensembles. Therefore, the cortical representation of vibration speed could underlie texture discrimination.

Experience-dependent changes in vibrissae evoked responses in the rodent barrel cortex.

A change in vibrissae complement in rodents leads to long-term changes in vibrissae dominance. These changes involve both potentiation of spared vibrissae responses and suppression of deprived vibrissae responses in adolescent animals. In adult animals only potentiation of spared vibrissae responses was detected. Suppression exhibits hetero- and homosynaptic components and appears to be cortical in origin, as is potentiation. The time course for potentiation and suppression in the barrel cortex of adolescent rats is different, with suppression preceeding potentiation by at least one week. There seems to be no critical period for potentiation in superficial layers of barrel cortex, but there is a critical period for suppression. Suppression cannot be evoked if plasticity is induced later than at 6 months of age nor maintained if experimental manipulations begin later than at three months. The molecular mechanisms that underlie plastic changes in the barrel cortex still remain unclear, although alpha-CamKII and to lesser extend alpha/beta-CREB appear to be involved.

Flow of excitation within rat barrel cortex on striking a single vibrissa.

1. Extracellular spike recordings were made from single cells in various layers of barrel cortex in adult rats anesthetized with urethan. Response magnitude and latency differences to brief 1.14 degrees deflections of mystacial vibrissae of center (principal) and surround receptive-field vibrissae were measured. Latency differences for pairs of cells in the same penetration to stimulation of the principal vibrissa were also collected. In separate experiments the domains of layer IV cells were mapped for their influence by a single vibrissa and their latencies to this vibrissa were recorded. In all experiments precise locations of layer IV cells in each penetration were identified using dye-lesioning and cytochrome oxidase staining of tangential sections. 2. The results suggest that principal vibrissa data are relayed radially in a column of neurons before parallel relay to adjacent columns. To the principal vibrissa, layers IV and Vb neurons discharged earliest, with layers II and III on average 2 and 3 ms later, respectively. Serial relay from layers IV to III to II was suggested to be the most common event. Although layer Va cells fired next, a single-column organization is not suggested for them because differences in latency or response magnitude to their principal and immediate surround vibrissae were not significant. Layer II, III and IV cells showed no statistical difference in latency to the nearest surround vibrissa but fired significantly later than to their principal input. 3. Because, from our previous studies, surround receptive fields of barrel cells in rat S1 cortex appear to be constructed intracortically, these data suggest a parallel column-column relay for their construction. Horizontal relay between barrels occurred first within the septae between barrels. Mean intracortical transmission velocities were calculated at approximately 0.05 m/s for column-column information transfer.