Sensing and processing whisker deflections in rodents

Abstract

The classical view of sensory information mainly flowing into barrel cortex at layer IV, moving up for complex feature processing and lateral interactions in layers II and III, then down to layers V and VI for output and corticothalamic feedback is becoming increasingly undermined by new evidence. We review the neurophysiology of sensing and processing whisker deflections, emphasizing the general processing and organisational principles present along the entire sensory pathway—from the site of physical deflection at the whiskers to the encoding of deflections in the barrel cortex. Many of these principles support the classical view. However, we also highlight the growing number of exceptions to these general principles, which complexify the system and which investigators should be mindful of when interpreting their results. We identify gaps in the literature for experimentalists and theorists to investigate, not just to better understand whisker sensation but also to better understand sensory and cortical processing.

Temporal activity patterns of layer II and IV rat barrel cortex neurons in healthy and injured conditions

“…In healthy conditions, layer II units largely reflect the same sorts of temporal activity patterns as are seen in layer IV and in almost the same proportions. This is slightly surprising given the layers serve markedly different functions (Burns & Rajan, 2021 )—the main layer IV excitatory output is to layers II and III whereas the layer II excitatory output is laterally to other parts of layer II (typically over several barrel columns), to other cells in layers III and V, and to secondary somatosensory and motor cortices (Aronoff et al, 2010 ; Feldmeyer et al, 2006 ). However, although the temporal activity patterns may be similar between layers II and IV, such patterns are not necessarily (and in fact unlikely to be) processed similarly.…”

“…The non‐stationarity of components could be an important feature to measure since, for units which had more than one component, some components appeared to interact, for example, while ascending in amplitude one component might increase its activity while the other simultaneously and proportionally decreases (e.g., left panel of Figure 2a ). Such interactions, if sufficiently separated in time, could be evidence of feedforward inhibition or disinhibition, known to be present, for example, in layer IV of barrel cortex (Burns & Rajan, 2021 ). To identify these features, we developed a novel graph‐theoretic analysis.…”

“…Such methods have been used to study pooled neural population responses in TBI barrel cortex models (Allitt, Iva, et al, 2016 ; Allitt, Johnstone, et al, 2016 ; Alwis et al, 2012 , 2013 , 2016 ; Alwis & Rajan, 2014 ; Carron, Alwis, et al, 2016 ; Carron, Yan, et al, 2016 ; Johnstone et al, 2013 , 2014 , 2015 ; Yan et al, 2013 ). Barrel cortex is an especially rich sensory area to study due to its ecological importance for rodents and the ability interpret and connect results to the significant number of past studies (Burns & Rajan, 2021 ). It is conveniently arranged into primary cortical columns which process the sensory information from individual whiskers from the rodent face, and the arrangement of these columns in barrel cortex maps to the arrangement of whiskers on the face.…”

“…For four reasons, we here focus only on layers II and IV:(1) layers II and IV have a very different proportions and types of interneurons (Markram et al, 2004 ), which are known to be affected differently by diffuse TBI (Carron, Alwis, et al, 2016 ); (2) layer IV is the main input layer and layer II is one of the first and most sophisticated signal processing layers in barrel cortex (Burns & Rajan, 2021 ); (3) data from TBI‐affected rats consistently show more superficial layers have medium‐ and long‐term changes in their excitability compared to deeper layers (Allitt, Iva, et al, 2016 ; Johnstone et al, 2013 ); and (4) recordings of layers II and IV have been the most frequent in past studies of TBI barrel cortex. Future studies may extend our analyses to other layers.…”

“…Future studies may extend our analyses to other layers. Although we do not perform waveform analysis or otherwise attempt to identify units as “fast spiking” or “regular spiking,” in relation to reason (1) above, we expected units from layer II to show greater perturbations to their temporal responses properties than layer IV given interneurons’ strong influence in various temporal coding schema in barrel cortex (Burns & Rajan, 2021 ; Markram et al, 2004 ).…”