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Spiking in Primary Somatosensory Cortex During Natural Whisking in Awake Head-Restrained Rats Is Cell-Type Specific

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Spiking in Primary Somatosensory Cortex During Natural Whisking in Awake Head-Restrained Rats Is Cell-Type Specific Spiking in primary somatosensory cortex during natural whisking in awake head-restrained rats is cell-type specific Christiaan P. J. de Kocka,b,1 and Bert Sakmannc,1 aDepartment of Neuroscience, Erasmus Medical Center, Dr. Molewaterplein 50, NL-3015 GE Rotterdam, The Netherlands; bDepartment of Integrative Neurophysiology, Vrije Universiteit Amsterdam, de Boelelaan 1085, NL-1081 HV Amsterdam, The Netherlands; and cMax-Planck Institute of Neurobiology, Am Klopferspitz 18, D-82152 Martinsried, Germany Contributed by Bert Sakmann, June 8, 2009 (sent for review April 9, 2009) Sensation involves active movement of sensory organs, but it Results remains unknown how position or movement of sensory organs is Spiking Frequencies of Neurons in Awake Barrel Cortex. We recorded encoded in cortex. In the rat whisker system, each whisker is juxtasomally in different layers of barrel cortex of unanesthetized, represented by an individual cortical (barrel) column. Here, we head-fixed Wistar rats to record spiking frequencies of single quantified in awake, head-fixed rats the impact of natural whisker neurons while tracking whisker position (Fig. 1, Fig. S1). Because movements on action potential frequencies of single (identified) cortical layers contain multiple cell types (17, 18), recorded neurons neurons located in different layers of somatosensory (barrel) were labeled with biocytin for posthoc identification. Throughout cortex. In all layers, we found only weak correlations between the different layers (e.g., L2/3–L6), we recorded from neurons with spiking and whisker position or velocity. Conversely, whisking irregular spiking patterns with average values in the range of 0.1–6 significantly increased spiking rate in a subset of neurons located Hz (e.g., a supragranular pyramidal neuron in Fig. S1). The preferentially in layer 5A. This finding suggests that whisker frequency of spiking was significantly lower than the whisking movement could be encoded by population responses of neurons frequency, which typically showed a peak in the power spectrum in within all layers and by single slender-tufted pyramids in layer 5A. the range of 5–8 Hz (Fig. S1C). In addition, we did not find a correlation between occurrence of spikes and whisker position for barrel cortex ͉ identified cells ͉ action potential ͉ morphology this supragranular pyramid (Fig. S1B). However, we also recorded from pyramidal neurons that significantly increased spiking upon whisking (Fig. 1A). These neurons were preferentially located in the ctive scanning of the environment for sensory signals in- upper portion of the infragranular layer (L5A). In total, we creases resolution (1), but in turn affects signal represen- A recorded from 88 neurons throughout different cortical layers and tation due to modulatory influences linked to arousal (2, 3) and identified 26 neurons posthoc. Labeled neurons were classified through representation of movement-related signals in the sen- according to their location with respect to the cytochrome oxidase sory pathway (4). The whisker system of rodents is convenient to dense region, characteristic of granular L4 and were categorized as study cortical representation of sensory stimuli, because indi- supragranular pyramids, granular spiny neurons, slender-tufted, vidual whiskers on the face are represented functionally and thick-tufted, or L6 pyramids (Fig. 1B; for detailed description of anatomically by identifiable individual cortical columns (5, 6) classification criteria, see ref. 18; see Fig. 1C for all recording and whisker movements are readily accessible for video tracking. locations). Unlabeled neurons were also included and categorized Movement-related information of the whiskers arrives in sensory into layers according to recording depth (18). cortex through activation of the sensory pathway by mechano- To study whether spiking correlated to behavioral state, we receptors in the whisker follicle (7, 8); although corollary compared spiking in anesthetized animals with spiking in awake, discharge (or efferent copy) through a monosynaptic pathway head-fixed animals (Fig. 1 D–G). In anesthetized animals, spik- from motor cortex (9) can also affect spiking in sensory cortex ing frequency was low (0.1–1 Hz), with the exception of thick- (7). With respect to the sensory pathway of the trigeminal tufted pyramids (Fig. 1D). Average spiking frequencies under system, it has been suggested that whisker movement and urethane were (in Hz Ϯ SD): supragranular pyramids 0.39 Ϯ whisker contact are encoded by different parallel pathways (10). 0.56 (n ϭ 22), granular spiny neurons 0.58 Ϯ 0.36 (n ϭ 15), Movement is encoded via the paralemniscal pathway [and slender-tufted pyramids 1.08 Ϯ 0.38 (n ϭ 16), thick-tufted possibly through a recent described pathway involving ventro- pyramids 3.27 Ϯ 1.62 (n ϭ 23), and L6 pyramids 0.47 Ϯ 0.46 (n ϭ posterior medial nucleus of thalamus (11)]. Contact is encoded 15) (18, 19). During quiet (nonwhisking) episodes in awake, via the extralemniscal pathway. The lemniscal pathway is head-fixed animals, spiking frequencies of identified neurons thought to participate in encoding both movement and contact. were comparable to those in urethane anesthesia (Fig. 1E,in These experiments, however, were conducted in anesthetized Hz Ϯ SD): supragranular pyramids 0.31 Ϯ 0.21 (n ϭ 5), granular animals, and whisking was evoked by electrical nerve stimulation spiny neurons 1.93 Ϯ 2.02 (n ϭ 9), slender-tufted pyramids (10). In addition, recent thalamic recordings in anesthetized and 1.62 Ϯ 1.81 (n ϭ 3), thick-tufted pyramids 4.12 Ϯ 3.22 (n ϭ 5), awake animals challenged the view that the paralemniscal and L6 pyramids 0.52 Ϯ 0.47 (n ϭ 4). During episodes of whisker pathway is encoding whisker movement (12, 13). Finally, cortical movement, individual neurons showed variable and layer specific recordings in awake animals during free whisking showed that changes in spiking frequency (up to 14 Hz, Fig. 1F). Average movement-related information is only weakly encoded in most, but not all neurons in sensory cortex (7, 14). But because Author contributions: C.P.J.d.K. and B.S. designed research, performed research, analyzed recorded neurons were not identified posthoc, the contribution data, and wrote the paper. of specific cell-types in encoding movement-related information The authors declare no conflict of interest. during active whisking remains unknown. Thus, although corti- 1To whom correspondence may be addressed. E-mail: [email protected] or cal neurons excited by the paralemniscal pathway (e.g., Layer [email protected]. 5A) (15, 16) may be involved in encoding of whisker movement, This article contains supporting information online at www.pnas.org/cgi/content/full/ this involvement actually remains to be established. 0904143106/DCSupplemental. 16446–16450 ͉ PNAS ͉ September 22, 2009 ͉ vol. 106 ͉ no. 38 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0904143106 Downloaded by guest on September 29, 2021 A A quiet whisking B L5A recording 1 15 decreased spiking supragr. gr. spiny gr. star increased spiking APs pyramid stellate pyramid no change 3 mV 10 supragr. pyr. 25 degrees gr. spiny neuron 5 10 5 slender-t. pyr. 5 sec 1 thick-t. pyr. WP 5 L6 pyr. protraction Spiking frequency (Hz) Cumulative probability slender-t. thick-t. L6 0 B 25 5 10 0 500 1000 1500 2000 supragr. granular granular slender- thick- L6 µ pyramid spiny star tufted tufted pyramid Spiking frequency (Hz) Recording depth ( m) stellate pyramid pyramid pyramid C E1 C D 15 decreased spiking decreased spiking increased spiking increased spiking 100 C1 no change L2/3 L4 L5A L5B L6 A1 10 supragr. pyr. 50 gr. spiny neuron 400 µm septal septal slender-t. pyr. 200 µm thick-t. pyr. 0 5 L6 pyr. unidentified -50 during whisking (%) Spiking frequency (Hz) sign. change in spiking Fraction of neurons with DFurethane E awake, quiet awake, whisking G 0 -100 all units 0 500 1000 1500 2000 15 supragr. pyr. thick-t. pyr. 5 0 500 1000 1500 2000 gr. spiny n. L6 pyr. Recording depth (µm) Recording depth (µm) 10 slender-t. pyr. unidentified L5B 3 L5A Fig. 2. Effect of behavioral state on cortical spiking is layer-specific. (A) 5 L4 Cumulative histograms of spiking activity for individual quiet and whisking 1 L6 Spont. act. (Hz) L2/3 episodes for examples illustrated in Fig. 1B (except thick-tufted neuron). (B 1000 2000 1000 2000 1000 2000 spont. act. (Hz) Avg. and C) Correlation of spiking frequency during quiet and whisking episodes Recording depth (µm) awake with respect to recording depth for identified neurons only (B) or all recorded urethane quiet awake whisking units (C). Connected symbols represent individual experiments. Red solid bar indicates a significant increase in spiking activity during whisking, green solid Fig. 1. Spiking frequencies of neurons in awake barrel cortex. (A) Spiking bar indicates a significant decrease in spiking activity during whisker move- NEUROSCIENCE (band-pass filtered from 300–9,000 Hz) and whisker position (WP) during ment, and dashed bars indicate no significant difference. (D) Fraction of juxtasomal recording of a L5A neuron in somatosensory cortex. (B) Neuro- recorded units (in %) that significantly changed spiking activity upon whisking lucida reconstructions of representative examples in coronal view. Gray con- as a function of recording depth. Green indicates decreased spiking activity tours illustrate barrel contours (see Fig. 1C ). Thick-tufted pyramid was re- and red indicates increased spiking activity, respectively. Bin size, 250 ␮m; corded in D2 column of urethane anesthetized animal. (C ) Tangential view of smooth curve represents the fraction calculated for individual bins that sig- barrel cortex (example map) with collected recording locations. (D–F ) Spon- nificantly increased (red) or decreased (green) spiking. taneous activity versus recording depth for neurons recorded under anesthe- tized conditions (D), awake and quiet (E ), or awake and whisking (F ), respec- tively. (G) Average spiking frequency for all units during different behavioral states.
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