Barrel cortex and whisker-mediated behaviors

Current Opinion in Neurobiology

Volumn 17, Issue 4, 2007, Pages 408-416

  Brecht, Michael ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL POPULATION; GRANULAR CELL; MEDIAL LEMNISCUS; NERVE CELL NETWORK; NERVE POTENTIAL; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RECOGNITION; REVIEW; SOMATOSENSORY CORTEX; STIMULUS RESPONSE; TACTILE STIMULATION; THALAMOCORTICAL TRACT; THALAMUS; VIBRISSA;

ANIMALS; BEHAVIOR, ANIMAL; MODELS, NEUROLOGICAL; NERVE NET; NEURAL PATHWAYS; NONLINEAR DYNAMICS; SOMATOSENSORY CORTEX; SYNAPTIC TRANSMISSION; VIBRISSAE;

EID: 34948849153     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2007.07.008     Document Type: Review

References (64)

1. Feldman D.E., and Brecht M. Map plasticity in somatosensory cortex. Science 310 (2005) 810-815
2. Kleinfeld D., Ahissar E., and Diamond M.E. Active sensation: insights from the rodent vibrissa sensorimotor system. Curr Opin Neurobiol 16 (2006) 435-444
3. Finnerty G.T., Roberts L.S., and Connors B.W. Sensory experience modifies the short-term dynamics of neocortical synapses. Nature 400 (1999) 367-371
4. Lu S.M., and Lin R.C. Thalamic afferents of the rat barrel cortex: a light- and electron-microscopic study using Phaseolus vulgaris leucoagglutinin as an anterograde tracer. Somatosens Motor Res 10 (1993) 1-16
5. Diamond M.E. Somatosensory thalamus of the rat. In: Jones E.G., and Diamond I.T. (Eds). The Barrel Cortex of Rodents (1995), Plenum Press 189-219
6. Sharp F.R., and Evans K. Regional (14C) 2-deoxyglucose uptake during vibrissae movements evoked by rat motor cortex stimulation. J Comp Neurol 208 (1982) 255-287
7. Yu C., Derdikman D., Haidarliu S., and Ahissar E. Parallel thalamic pathways for whisking and touch signals in the rat. PLoS Biol 4 (2006) e124
8. Louderback K.M., Glass C.S., Shamalla-Hannah L., Erickson S.L., and Land P.W. Subbarrel patterns of thalamocortical innervation in rat somatosensory cortical barrels: organization and postnatal development. J Comp Neurol 497 (2006) 32-41
9. Andermann M.L., and Moore C.I. A somatotopic map of vibrissa motion direction within a barrel column. Nat Neurosci 4 (2006) 543-551
10. Bruno R.M., Khatri V., Land P.W., and Simons D.J. Thalamocortical angular tuning domains within individual barrels of rat somatosensory cortex. J Neurosci 23 (2003) 9565-9574
11. Kim U., and Ebner F.F. Barrels and septa: separate circuits in rat barrels field cortex. J Comp Neurol 408 (1999) 489-505
12. Brecht M., Roth A., and Sakmann B. Dynamic receptive fields of reconstructed pyramidal cells in layers 3 and 2 of the rat somatosensory cortex. J Physiol 553 (2003) 243-265
13. Brecht M., and Sakmann B. Dynamic representation of whisker deflection by synaptic potentials in spiny stellate and pyramidal cells in the barrels and septa of layer 4 rat somatosensory cortex. J Physiol 543 (2002) 49-70
14. Lübke J., Egger V., Sakmann B., and Feldmeyer D. Columnar organization of dendrites and axons of single and synaptically coupled excitatory spiny neurons in layer 4 of the rat barrel cortex. J Neurosci 20 (2000) 5300-5311
15. Ahissar E., Sosnik R., and Haidarliu S. Transformation from temporal to rate coding in a somatosensory thalamocortical pathway. Nature 406 (2000) 302-306
16. Manns I.D., Sakmann B., and Brecht M. Sub- and suprathreshold receptive field properties of pyramidal neurons in layers 5A and 5B of rat somatosensory barrel cortex. J Physiol 556 (2004) 601-622
17. Schubert D., Kotter R., Luhmann H.J., and Staiger J.F. Morphology, electrophysiology and functional input connectivity of pyramidal neurons characterizes a genuine layer va in the primary somatosensory cortex. Cereb Cortex 16 (2006) 223-236. The authors use photostimulation/glutamate uncaging to derive detailed input maps for layer 5A neurons. The authors demonstrate a direct input from layer 4 barrels to layer 5A cells, which implies that layer 5A is a site of convergence of leminscal inputs (from layer 4 barrels) and paralemniscal inputs (from POM thalamus).
18. Bureau I., von Saint Paul F., and Svoboda K. Interdigitated paralemniscal and lemniscal pathways in the mouse barrel cortex. PLoS Biol 4 (2006) e382. The authors examine how leminscal inputs and paralemniscal inputs map onto the architecture of barrel cortex.
19. Feldmeyer D., Roth A., and Sakmann B. Monosynaptic connections between pairs of spiny stellate cells in layer 4 and pyramidal cells in layer 5A indicate that lemniscal and paralemniscal afferent pathways converge in the infragranular somatosensory cortex. J Neurosci 25 (2005) 3423-3431
20. Ito M. Simultaneous visualization of cortical barrels and horseradish peroxidase injected layer 5b vibrissa neurons in the rat. J Physiol 454 (1992) 247-265
21. Markram H., Lübke J., Frotscher M., Roth A., and Sakmann B. Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol 500 (1997) 409-440
22. Feldmeyer D., Egger V., Lübke J., and Sakmann B. Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single 'barrel' of developing rat somatosensory cortex. J Physiol 521 (1999) 169-190
23. Feldmeyer D., Lübke J., and Sakmann B. Efficacy and connectivity of intracolumnar pairs of layer 2/3 pyramidal cells in the barrel cortex of juvenile rats. J Physiol 575 (2006) 583-602
24. Cowan A.I., and Stricker C. Functional connectivity in layer IV local excitatory circuits of rat somatosensory cortex. J Neurophysiol 92 (2004) 2137-2150
25. Bruno R.M., and Sakmann B. Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312 (2006) 1622-1627. The authors combine thalamic extracellular recordings with in vivo whole-cell recordings in cortical layer 4 and are thus for the first time able to directly measure thalamocortical unitary connections. The findings indicate that thalamocortical unitary connections are of small amplitude (a PSP amplitude of ∼0.5 mV) and that a substantial fraction of thalamic afferents to a layer 4 neuron is required to drive a cortical neuron across threshold.
26. Brecht M., and Sakmann B. Whisker maps of neuronal subclasses of the rat ventral posterior medial thalamus, identified by whole-cell voltage recording and morphological reconstruction. J Physiol 538 (2002) 495-515
27. Gentet L.J., and Ulrich D. Strong, reliable and precise synaptic connections between thalamic relay cells and neurones of the nucleus reticularis in juvenile rats. J Physiol 546 (2003) 801-811
28. Waters J., and Helmchen F. Background synaptic activity is sparse in neocortex. J Neurosci 26 (2006) 8267-8277. This paper reports an extremely thorough investigation of the synaptic input impinging on a cortical neuron in vivo during network states with increased activity (Up states) and during network states with decreased activity (Down states). The authors find that background activity is low, overall synaptic currents are small and that the shunting of responses by synaptic channels is counteracted by anomalous rectification, resulting in a net increase in input resistance during Up states. The work is both surprising and compelling.
29. Brecht M., Schneider M., and Manns I. Silent neurons in sensorimotor cortices: implications for plasticity. In: Ebner (Ed). Neural Plasticity in Adult Somatic Sensory-Motor Systems (2005), CRC Press 1-19
30. Moore C.I., and Nelson S.B. Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J Neurophysiol 80 (1998) 2882-2892
31. Zhu J.J., and Connors B.W. Intrinsic firing patterns and whisker-evoked synaptic responses of neurons in the rat barrel cortex. J Neurophysiol 81 (1999) 1171-1183
32. Margrie T.W., Brecht M., and Sakmann B. In vivo, low-resistance, whole-cell recordings from neurons in the anaesthetized and awake mammalian brain. Pflugers Arch 444 (2002) 491-498
33. Simons D.J. Response properties of vibrissa units in rat SI somatosensory neocortex. J Neurophysiol 41 (1978) 798-820
34. Simons D.J., and Carvell G.E. Thalamocortical response transformations in the rat vibrissa/barrel system. J Neurophysiol 61 (1989) 311-330
35. Pinto D.J., Brumberg J.C., and Simons D.J. Circuit dynamics and coding strategies in rodent somatosensory cortex. J Neurophysiol 83 (2000) 1158-1166
36. Gabernet L., Jadhav S.P., Feldman D.E., Carandini M., and Scanziani M. Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition. Neuron 48 (2005) 315-327. The authors use an in vitro approach to determine how inhibition shapes the integration time of neurons in barrel cortex.
37. Sun Q.Q., Huguenard J.R., and Prince D.A. Barrel cortex microcircuits: thalamocortical feedforward inhibition in spiny stellate cells is mediated by a small number of fast-spiking interneurons. J Neurosci 26 (2006) 1219-1230. The authors characterize the inhibitory cell population in layer 4 barrels and identify the fast-spiking interneuron population as the major mediator of feed-forward inhibition in the barrels.
38. Cruikshank S.J., Lewis T.J., and Connors B.W. Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex. Nat Neurosci 10 (2007) 462-468. A detailed analysis of cellular mechanisms underlying the recruitment of fast rising inhibition by thalamic afferents.
39. Wilent W.B., and Contreras D. Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex. Nat Neurosci 8 (2005) 1364-1370. The authors analyze barrel cortex responses to whisker deflection of different directions by intracellular recordings. They argue that the timing rather than the amplitude of excitatory and inhibitory inputs determines tuning.
40. Castro-Alamancos M.A. Dynamics of sensory thalamocortical synaptic networks during information processing states. Prog Neurobiol 74 (2004) 213-247
41. Chung S., Li X., and Nelson S.B. Short-term depression at thalamocortical synapses contributes to rapid adaptation of cortical sensory responses in vivo. Neuron 34 (2002) 437-446
42. Katz Y., Heiss J.E., and Lampl I. Cross-whisker adaptation of neurons in the rat barrel cortex. J Neurosci 26 (2006) 13363-13372
43. Maravall M., Petersen R.S., Fairhall A.L., Arabzadeh E., and Diamond M.E. Shifts in coding properties and maintenance of information transmission during adaptation in barrel cortex. PLoS Biol 5 (2007) e19. This study investigates the effects of changing stimulus statistics on barrel cortex neurons. Accordingly barrel cortex neurons show rate adaptation and their input-output tuning function scales with the changes in stimulus distribution.
44. Petersen R.S., Panzeri S., and Diamond M.E. Population coding of stimulus location in rat somatosensory cortex. Neuron 32 (2001) 503-514
45. Petersen R.S., Panzeri S., and Diamond M.E. The role of individual spikes and spike patterns in population coding of stimulus location in rat somatosensory cortex. Biosystems 67 (2002) 187-193
46. Mokeichev A., Okun M., Barak O., Katz Y., Ben-Shahar O., and Lampl I. Stochastic emergence of repeating cortical motifs in spontaneous membrane potential fluctuations in vivo. Neuron 53 (2007) 413-425. The authors search for and find repeating patterns of cortical activity in intracellular recordings from rat barrel cortex. However, the comparison of these patterns to stochastically generated surrogate data points to a random (by chance) origin of these patterns.
47. Ikegaya Y., Aaron G., Cossart R., Aronov D., Lampl I., Ferster D., and Yuste R. Synfire chains and cortical songs: temporal modules of cortical activity. Science 304 (2004) 559-564
48. Ferezou I., Bolea S., and Petersen C.C. Visualizing the cortical representation of whisker touch: voltage-sensitive dye imaging in freely moving mice. Neuron 50 (2006) 617-629
49. Lee A.K., Manns I.D., Sakmann B., and Brecht M. Whole-cell recordings in freely moving rats. Neuron 51 (2006) 399-407
50. Brecht M., Preilowski B., and Merzenich M.M. Functional architecture of the mystacial vibrissae. Behav Brain Res 84 (1997) 81-97
51. Guic-Robles E., Valdivieso C., and Guajardo G. Rats can learn a roughness discrimination using only their vibrissal system. Behav Brain Res 31 (1989) 285-289
52. Simons D.J. Neuronal integration in the somatosensory whisker/barrel cortex. In: Jones E.G., and Diamond I.T. (Eds). The Barrel Cortex of Rodents (1995), Plenum Press 262-298
53. Carvell G.E., and Simons D.J. Biometric analyses of vibrissal tactile discrimination in the rat. J Neurosci 10 (1990) 2638-2648
54. Arabzadeh E., Zorzin E., and Diamond M.E. Neuronal encoding of texture in the whisker sensory pathway. PLoS Biol 3 (2005) e17
55. Stuttgen M.C., Ruter J., and Schwarz C. Two psychophysical channels of whisker deflection in rats align with two neuronal classes of primary afferents. J Neurosci 26 (2006) 7933-7934. The investigators analyze detection of whisker deflection in rats. The results suggest two psychophysical channels for detection, which may correspond to slowly adapting and rapidly adapting classes of afferents.
56. Krupa D.J., Matell M.S., Brisben A.J., Oliveira L.M., and Nicolelis M.A. Behavioral properties of the trigeminal somatosensory system in rats performing whisker-dependent tactile discriminations. J Neurosci 21 (2001) 5752-5763
57. Knutsen P.M., Pietr M., and Ahissar E. Haptic object localization in the vibrissal system: behavior and performance. J Neurosci 26 (2006) 8451-8464. This study analyzes the ability of rats to report horizontal object position.
58. Mehta S.B., Whitmer D., Figueroa R., Williams B.A., and Kleinfeld D. Active spatial perception in the vibrissa scanning sensorimotor system. PLoS Biol 5 (2007) e15. This interesting study demonstrates the ability of rats to report horizontal object position with only a single intact whisker.
59. Mitchinson B., Martin C.J., Grant R.A., and Prescott T.J. Feedback control in active sensing: rat exploratory whisking is modulated by environmental contact. Proc Biol Sci 274 (2007) 1035-1041. In this article the investigators report on whisker movements and whisker contacts in free ranging blind rats. The investigators show that rats have a pronounced tendency to minimize the impingement of whiskers in obstacle collisions. A most beautiful study that reminds us how little we know about whisker movements even in very simple settings.
60. Nguyen Q.T., and Kleinfeld D. Positive feedback in a brainstem tactile sensorimotor loop. Neuron 45 (2005) 447-457
61. Towal R.B., and Hartmann M.J. Right-left asymmetries in the whisking behavior of rats anticipate head movements. J Neurosci 26 (2006) 8838-8846
62. Catania K.C., and Remple F.E. Asymptotic prey profitability drives star-nosed moles to the foraging speed limit. Nature 433 (2005) 519-522. This study documents tactile behaviors of the star-nosed moles. The handling of prey occurs breathtakingly fast.
63. Anjum F., Turni H., Mulder P.G., van der Burg J., and Brecht M. Tactile guidance of prey capture in Etruscan shrews. Proc Natl Acad Sci USA 103 (2006) 16544-16549. In this study whisker-mediated prey capture was studied in the Etruscan shrew. This is one of the smallest mammals, and it attacks crickets almost as big as itself. Prey capture behavior relies completely on tactile shape cues.
64. Kwegyir-Afful E.E., and Keller A. Response properties of whisker-related neurons in rat second somatosensory cortex. J Neurophysiol 92 (2004) 2083-2092