Toward Behavioral Benchmarks for Whisker-Related Sensory Processing

Review of O’Connor et al.The rodent whisker-to-barrel pathwayservesasamajormodelsystemfortheinves-tigation of sensorimotor processing. Its keyadvantage is a well defined topographicmap,inwhicheachoftheorderlyarrangedwhiskers on the snout of the animal is pro-cessedlargelyinacorrespondingfunctionalcolumn in primary somatosensory (“bar-rel”) cortex. This topographic map is situ-atedontopofalissencephaliccortex,andisthuseasilyaccessibleforelectrodesorimag-ing microscopes. The map can be easily al-tered, e.g., by plucking whiskers duringdifferent stages of brain development, al-lowingstudyofplasticitymechanisms.Fur-thermore, rodents use their whiskers forexploration in a highly active manner,rhythmicallysweepingthembackandforth(“whisking”), which provides the opportu-nity to study sensorimotor integration in asystem with considerably fewer degrees offreedomthanprimatehands.Althoughbarrelcortexiswell describedin terms of microcircuitry (Lu¨bke andFeldmeyer, 2007) and mechanisms of plas-ticity(FeldmanandBrecht,2005),thereisapaucityofbehavioraldataonwhiskerusage.Whileratsclearlycanusetheirwhiskersforobjectlocalization(HutsonandMasterton,1986) and texture discrimination (Carvelland Simons, 1990), little is known abouthow the animals employ their whiskers toaccomplish these tasks. This situation islargely because of a lack of methods thatallow precise quantification of whiskermovements while, at the same time, per-mitting psychophysical assessments. Theintricate interplay of whiskers and surfacesduring free exploration calls for analysiswith millisecond resolution and microme-ter precision and can most accurately beexamined using high-speed videography,whichinturnrequiressophisticatedanal-ysissoftwaretotracksinglewhiskers(Rittet al., 2008). Because of the lack of psychophysicalwhisker-based paradigms and the difficul-ties in measuring whisking, experimentsandtheoriesonwhiskersensoryprocessinghave been largely unconstrained by behav-ioral benchmarks. For example, investiga-torshaveroutinelystimulatedwhiskerswithamplitudesandvelocitiesthathaverecentlybeen found to be on the lower end of thespectrumratsencounterduringexploration(Ritt et al., 2008) and, in fact, are occasion-ally close to absolute perceptual threshold(Stu¨ttgenetal.,2006). Similarly,somestud-ies have presented stimuli (e.g., surfaces ofdiffering roughness like sandpapers) to thewhiskersthathavenotbeenshowntobedis-criminablebytrainedanimals.In a similar vein, a recent study com-pared the information contents of spikecount versus the spikes’ temporal patternforwhisker-basedtexturediscriminationinanesthetized animals (Arabzadeh et al.,2006),andfoundthatanalysisofspikepat-terns allows better discriminability of tex-tures than analysis of spike counts. Thisfindingmaybetakentosuggestthattheratdoesindeedbaseitscapacityfortexturedis-crimination on spike patterns, but is notconclusiveofthecodingsymbolthatisused.Also, it is not known how well trained ani-mals can distinguish between the stimulitheseauthorspresented.However,combin-ingneuralrecordingswithabehavioraltaskmaysolvethisissue,ashasbeendoneintheprimate tactile system. Herna´ndez et al.(2000) found that, similar to the whiskersystem,thetemporalpatternsofspiketrains(periodicity) in primary somatosensorycortex provided more information aboutthe frequency of a vibrotactile signal thanspike counts, thus permitting superior dis-criminationperformance.However,neuro-metricdiscriminabilitybasedonperiodicityby far exceeded the discriminability shownbytheanimals,whileneurometricdiscrim-inability based on spike counts yielded agood match to the psychometric data. Thisresultandadditionalcomparisonsofbehav-ioral and neuronal data led to the conclu-sion that the neural code for frequencydiscrimination is spike count rather thanspikeperiodicity(Lunaetal.,2005). Insummary,researchonneuralprocess-inginthewhiskersystemneedstobelinkedto behavioral benchmarks: which surfacesand objects can be discriminated, and howwell? Whatforcesimpingeonwhiskersdur-ing object localization or texture discrimi-nation? Whatstrategiesdoanimalsapplytomeet different task demands, and how dothese strategies affect neural processing atdifferent levels of the whisker-to-barrel