Laminar-specific encoding of texture elements in rat barrel cortex.

KEY POINTS: For rats texture discrimination is signalled by the large face whiskers by stick-slip events. Neural encoding of repetitive stick-slip events will be influenced by intrinsic properties of adaptation. We show that texture coding in the barrel cortex is laminar specific and follows a power function. Our results also show layer 2 codes for novel feature elements via robust firing rates and temporal fidelity. We conclude that texture coding relies on a subtle neural ensemble to provide important object information. ABSTRACT: Texture discrimination by rats is exquisitely guided by fine-grain mechanical stick-slip motions of the face whiskers as they encounter, stick to and slip past successive texture-defining surface features such as bumps and grooves. Neural encoding of successive stick-slip texture events will be shaped by adaptation, common to all sensory systems, whereby receptor and neural responses to a stimulus are affected by responses to preceding stimuli, allowing resetting to signal novel information. Additionally, when a whisker is actively moved to contact and brush over surfaces, that motion itself generates neural responses that could cause adaptation of responses to subsequent stick-slip events. Nothing is known about encoding in the rat whisker system of stick-slip events defining textures of different grain or the influence of adaptation from whisker protraction or successive texture-defining stick-slip events. Here we recorded responses from halothane-anaesthetized rats in response to texture-defining stimuli applied to passive whiskers. We demonstrate that: across the columnar network of the whisker-recipient barrel cortex, adaptation in response to repetitive stick-slip events is strongest in uppermost layers and equally lower thereafter; neither whisker protraction speed nor stick-slip frequency impede encoding of stick-slip events at rates up to 34.08 Hz; and layer 2 normalizes responses to whisker protraction to resist effects on texture signalling. Thus, within laminar-specific response patterns, barrel cortex reliably encodes texture-defining elements even to high frequencies.