Weaker feedforward inhibition accounts for less pronounced thalamocortical response transformation in mouse vs. rat barrels

Abstract

Kwegyir-Afful EE, Kyriazi HT, Simons DJ. Weaker feedforward inhibition accounts for less pronounced thalamocortical response transformation in mouse vs. rat barrels. J Neurophysiol 110: 2378 -2392, 2013. First published August 21, 2013 doi:10.1152/jn.00574.2012.-Feedforward inhibition is a common motif of thalamocortical circuits. Strong engagement of inhibitory neurons by thalamic inputs enhances response differentials between preferred and nonpreferred stimuli. In rat whisker-barrel cortex, robustly driven inhibitory barrel neurons establish a brief epoch during which synchronous or nearsynchronous thalamic firing produces larger responses to preferred stimuli, such as high-velocity deflections of the principal whisker in a preferred direction. Present experiments in mice show that barrel neuron responses to preferred vs. nonpreferred stimuli differ less than in rats. In addition, fast-spike units, thought to be inhibitory barrel neurons, fire less robustly to whisker stimuli in mice than in rats. Analyses of real and simulated data indicate that mouse barrel circuitry integrates thalamic inputs over a broad temporal window, and that, as a consequence, responses of barrel neurons are largely similar to those of thalamic neurons. Results are consistent with weaker feedforward inhibition in mouse barrels. Differences in thalamocortical circuitry between mice and rats may reflect mechanical properties of the whiskers themselves. cortical circuits; thalamus; whiskers SENSORY AREAS OF THE CEREBRAL cortex are strongly driven by thalamic inputs. Studies of visual and somatosensory systems offer compelling evidence for such feedforward models. Accumulating evidence suggests a common circuit motif of thalamocortical input to both excitatory and inhibitory neurons whose interactions alter or transform incoming sensory signals (Alonso and Swadlow 2005; Bruno 2011). Feedforward inputs establish initial cortical response tuning, whereas engagement of inhibitory neurons by thalamocortical inputs acts in conjunction with neuronal and circuit nonlinearities (Pesavento et al. 2010) to enhance response differentials between preferred and nonpreferred stimuli (Miller 2003;Miller et al. 2001). Thalamic inputs evoke short-latency excitation followed by inhibition, creating a limited temporal window for afferent signals to produce cortical spiking (Gabernet et al. 2005;Wehr and Zador 2003). Indeed, diverse evidence indicates that response tuning in thalamocortical circuits is strongly affected by thalamic response timing and firing synchrony (Blomquist et al. 2009; Bruno and Sakmann 2006;Cardin et al. 2010). It is likely that, within this overall operational framework, details of local circuitry reflect evolutionary differences in brain structure and function, as well as constraints imposed by the nature of afferent signals arising from different sensory systems in different species.Thalamocortical processing in the rat whisker/barrel system is highly sensitive to thalamic population input timing Wang et al. 2010). Strong feedforw...

Genetically expressed voltage sensor ArcLight for imaging large scale cortical activity in the anesthetized and awake mouse

“…Given the intrinsic ArcLight fluorophore reported rise-time, time between onset and peak, of 10 to 20 ms, 1,2,18 our observations here correspond well with published in vivo anesthetized cortical extracellular single unit activity in layer 2∕3 (Ref. 39) and simultaneously recorded LFP signals (see Fig. 4).…”

“…The two ON and OFF sensory peaks are representative of a well-documented velocity sensitivity of the rodent whisker somatosensory pathway. 30,39,53 Additionally, we found that ArcLight S1 cortical responses clearly resolved repetitive frequency-dependent inputs between the ranges of 2.5 to 20 Hz high-frequency [ Fig. 5(a), panel 6, 40 Hz] deflections produced an overall increase in fluorescence that failed to clearly follow the sensory input.…”

“…To determine the temporal capabilities of ArcLight to represent complex stimuli, we presented a range of inputs to the whisker and recorded the downstream evoked cortical fluorescent response. We selected complex inputs that have been commonly used in the rodent vibrissa system, 39,[49][50][51][52] and therefore, these stimuli represent an additional comparison to published traditional electrophysiological recordings. Again, mice were anesthetized under low isoflurane (Sec.…”

Mechanisms underlying a thalamocortical transformation during active tactile sensation

“…Rate models have been used to study cortical responses to fast-rising stimuli in the whisker system [ 8 , 61 ] and elsewhere [ 71 ]. These previous models of L4 aimed to account for fast cortical responses to passive whisker deflections [ 8 ], but rate models cannot reliably describe brief responses to rapidly-varying stimuli [ 76 ]. Moreover, in important aspects these models have opposite behavior to our experimental and modeling results and to the known anatomy and physiology of L4 circuits.…”

“…Sensory information enters the cortex through the thalamus. Transformations in thalamocortical circuits have mostly been studied in anesthetized animals with passive sensory stimuli [ 2 – 8 ] or with artificial whisking [ 9 ]. In the somatosensory system these studies have revealed subtle differences in receptive field structure across neurons in the thalamocortical circuit [ 2 – 4 ].…”