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Defining cortical frequency tuning with recurrent excitatory circuitry

Nature Neuroscience volume 10, pages 1594–1600 (2007)Cite this article

Abstract

Neurons in the recipient layers of sensory cortices receive excitatory input from two major sources: the feedforward thalamocortical and recurrent intracortical inputs. To address their respective functional roles, we developed a new method for silencing cortex by competitively activating GABAA while blocking GABAB receptors. In the rat primary auditory cortex, in vivo whole-cell recording from the same neuron before and after local cortical silencing revealed that thalamic input occupied the same area of frequency-intensity tonal receptive field as the total excitatory input, but showed a flattened tuning curve. In contrast, excitatory intracortical input was sharply tuned with a tuning curve that closely matched that of suprathreshold responses. This can be attributed to a selective amplification of cortical cells' responses at preferred frequencies by intracortical inputs from similarly tuned neurons. Thus, weakly tuned thalamocortical inputs determine the subthreshold responding range, whereas intracortical inputs largely define the tuning. Such circuits may ensure a faithful conveyance of sensory information.

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Figure 1: Specific silencing of local intracortical connections with a cocktail pharmacological method.
Figure 2: Changes in excitatory synaptic TRF after local cortical silencing.
Figure 3: Intracortical inputs are more sharply tuned than thalamocortical inputs.
Figure 4: Similarly tuned intracortical inputs sharpen the frequency tuning curve in layer 4.

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References

  1. Reid, R.C. & Alonso, J.M. Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378, 281–284 (1995).

    Article  CAS  Google Scholar 

  2. Ferster, D., Chung, S. & Wheat, H. Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature 380, 249–252 (1996).

    Article  CAS  Google Scholar 

  3. Chung, S. & Ferster, D. Strength and orientation tuning of the thalamic input to simple cells revealed by electrically evoked cortical suppression. Neuron 20, 1177–1189 (1998).

    Article  CAS  Google Scholar 

  4. Miller, L.M., Escabi, M.A., Read, H.L. & Schreiner, C.E. Functional convergence of response properties in the auditory thalamocortical system. Neuron 32, 151–160 (2001).

    Article  CAS  Google Scholar 

  5. Bruno, R.M. & Sakmann, B. Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312, 1622–1627 (2006).

    Article  CAS  Google Scholar 

  6. Douglas, R.J., Koch, C., Mahowald, M., Martin, K.A. & Suarez, H.H. Recurrent excitation in neocortical circuits. Science 269, 981–985 (1995).

    Article  CAS  Google Scholar 

  7. Somers, D.C., Nelson, S.B. & Sur, M. An emergent model of orientation selectivity in cat visual cortical simple cells. J. Neurosci. 15, 5448–5465 (1995).

    Article  CAS  Google Scholar 

  8. Miller, K.D., Pinto, D.J. & Simons, D.J. Processing in layer 4 of the neocortical circuit: new insights from visual and somatosensory cortex. Curr. Opin. Neurobiol. 11, 488–497 (2001).

    Article  CAS  Google Scholar 

  9. Alonso, J.M. & Swadlow, H.A. Thalamocortical specificity and the synthesis of sensory cortical receptive fields. J. Neurophysiol. 94, 26–32 (2005).

    Article  Google Scholar 

  10. Miller, L.M., Escabi, M.A., Read, H.L. & Schreiner, C.E. Spectrotemporal receptive fields in the lemniscal auditory thalamus and cortex. J. Neurophysiol. 87, 516–527 (2002).

    Article  Google Scholar 

  11. Miller, L.M., Escabi, M.A. & Schreiner, C.E. Feature selectivity and interneuronal cooperation in the thalamocortical system. J. Neurosci. 21, 8136–8144 (2001).

    Article  CAS  Google Scholar 

  12. Martinez, L.M. et al. Receptive field structure varies with layer in the primary visual cortex. Nat. Neurosci. 8, 372–379 (2005).

    Article  CAS  Google Scholar 

  13. Fox, K., Wright, N., Wallace, H. & Glazewski, S. The origin of cortical surround receptive fields studied in the barrel cortex. J. Neurosci. 23, 8380–8391 (2003).

    Article  CAS  Google Scholar 

  14. Kaur, S., Lazar, R. & Metherate, R. Intracortical pathways determine breadth of subthreshold frequency receptive fields in primary auditory cortex. J. Neurophysiol. 91, 2551–2567 (2004).

    Article  Google Scholar 

  15. Zhang, Y. & Suga, N. Corticofugal amplification of subcortical responses to single tone stimuli in the mustached bat. J. Neurophysiol. 78, 3489–3492 (1997).

    Article  CAS  Google Scholar 

  16. Chung, S. & Ferster, D. Strength and orientation tuning of the thalamic input to simple cells revealed by electrically evoked cortical suppression. Neuron 20, 1177–1189 (1998).

    Article  CAS  Google Scholar 

  17. Volgushev, M., Vidyasagar, T.R., Chistiakova, M., Yousef, T. & Eysel, U.T. Membrane properties and spike generation in rat visual cortical cells during reversible cooling. J. Physiol. (Lond.) 522, 59–76 (2000).

    Article  CAS  Google Scholar 

  18. Villa, A.E. et al. Corticofugal modulation of the information processing in the auditory thalamus of the cat. Exp. Brain Res. 86, 506–517 (1991).

    Article  CAS  Google Scholar 

  19. Yamauchi, T., Hori, T. & Takahashi, T. Presynaptic inhibition by muscimol through GABAB receptors. Eur. J. Neurosci. 12, 3433–3436 (2000).

    Article  CAS  Google Scholar 

  20. Porter, J.T. & Nieves, D. Presynaptic GABAB receptors modulate thalamic excitation of inhibitory and excitatory neurons in the mouse barrel cortex. J. Neurophysiol. 92, 2762–2770 (2004).

    Article  CAS  Google Scholar 

  21. Roerig, B. & Chen, B. Relationships of local inhibitory and excitatory circuits to orientation-preference maps in ferret visual cortex. Cereb. Cortex 12, 187–198 (2002).

    Article  CAS  Google Scholar 

  22. Marino, J. et al. Invariant computations in local cortical networks with balanced excitation and inhibition. Nat. Neurosci. 8, 194–201 (2005).

    Article  CAS  Google Scholar 

  23. Zhang, L.I., Bao, S. & Merzenich, M.M. Persistent and specific influences of early acoustic environments on primary auditory cortex. Nat. Neurosci. 4, 1123–1130 (2001).

    Article  CAS  Google Scholar 

  24. Bringuier, V., Chavane, F., Glaeser, L. & Fregnac, Y. Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. Science 283, 695–699 (1999).

    Article  CAS  Google Scholar 

  25. Zhang, L.I., Tan, A.Y., Schreiner, C.E. & Merzenich, M.M. Topography and synaptic shaping of direction selectivity in primary auditory cortex. Nature 424, 201–205 (2003).

    Article  CAS  Google Scholar 

  26. Wehr, M. & Zador, A.M. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426, 442–446 (2003).

    Article  CAS  Google Scholar 

  27. Tan, A.Y., Zhang, L.I., Merzenich, M.M. & Schreiner, C.E. Tone-evoked excitatory and inhibitory synaptic conductances of primary auditory cortex neurons. J. Neurophysiol. 92, 630–643 (2004).

    Article  Google Scholar 

  28. Carandini, M. & Ferster, D. Membrane potential and firing rate in cat primary visual cortex. J. Neurosci. 20, 470–484 (2000).

    Article  CAS  Google Scholar 

  29. Anderson, J.S., Carandini, M. & Ferster, D. Orientation tuning of input conductance, excitation and inhibition in cat primary visual cortex. J. Neurophysiol. 84, 909–926 (2000).

    Article  CAS  Google Scholar 

  30. Priebe, N. & Ferster, D. Direction selectivity of excitation and inhibition in simple cells of the cat primary visual cortex. Neuron 45, 133–145 (2005).

    Article  CAS  Google Scholar 

  31. Wilent, W.B. & Contreras, D. Stimulus-dependent changes in spike threshold enhance feature selectivity in rat barrel cortex neurons. J. Neurosci. 25, 2983–2991 (2005).

    Article  CAS  Google Scholar 

  32. Swadlow, H.A. & Gusev, A.G. Receptive-field construction in cortical inhibitory interneurons. Nat. Neurosci. 5, 403–404 (2002).

    Article  CAS  Google Scholar 

  33. Wu, G.K., Li, P., Tao, H.W. & Zhang, L.I. Nonmonotonic synaptic excitation and imbalanced inhibition underlying cortical intensity tuning. Neuron 52, 705–715 (2006).

    Article  CAS  Google Scholar 

  34. Winer, J.A., Miller, L.M., Lee, C.C. & Schreiner, C.E. Auditory thalamocortical transformation: structure and function. Trends Neurosci. 28, 255–263 (2005).

    Article  CAS  Google Scholar 

  35. Calford, M.B. & Webster, W.R. Auditory representation within principal division of cat medial geniculate body: an electrophysiology study. J. Neurophysiol. 45, 1013–1028 (1981).

    Article  CAS  Google Scholar 

  36. Moore, C.I. & Nelson, S.B. Spatio-temporal subthreshold receptive fields in the vibrissa representation of rat primary somatosensory cortex. J. Neurophysiol. 80, 2882–2892 (1998).

    Article  CAS  Google Scholar 

  37. Margrie, T.W., Brecht, M. & Sakmann, B. In vivo, low-resistance, whole-cell recordings from neurons in the anaesthetized and awake mammalian brain. Pflugers Arch. 444, 491–498 (2002).

    Article  CAS  Google Scholar 

  38. Games, K.D. & Winer, J.A. Layer V in rat auditory cortex: projections to the inferior colliculus and contralateral cortex. Hear. Res. 34, 1–25 (1988).

    Article  CAS  Google Scholar 

  39. Horikawa, K. & Armstrong, W.E. A versatile means of intracellular labelling: injection of biocytin and its detection with avidin conjugates. J. Neurosci. Methods 25, 1–11 (1988).

    Article  CAS  Google Scholar 

  40. Zhu, Y., Stornetta, R.L. & Zhu, J.J. Chandelier cells control excessive cortical excitation: characteristics of whisker-evoked synaptic responses of layer 2/3 nonpyramidal and pyramidal neurons. J. Neurosci. 24, 5101–5108 (2004).

    Article  CAS  Google Scholar 

  41. Hirsch, J.A., Alonso, J.M., Reid, R.C. & Martinez, L.M. Synaptic integration in striate cortical simple cells. J. Neurosci. 18, 9517–9528 (1998).

    Article  CAS  Google Scholar 

  42. Borg-Graham, L.J., Monier, C. & Fregnac, Y. Visual input evokes transient and strong shunting inhibition in visual cortical neurons. Nature 393, 369–373 (1998).

    Article  CAS  Google Scholar 

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Acknowledgements

HThis work was supported by grants to L.I.Z. from the US National Institutes of Health/National Institute on Deafness and Other Communication Disorders, the Searle Scholar Program, the Esther A. & and Joseph Klingenstein Fund, Inc., and the David and Lucile Packard Foundation.

Author information

Author notes

  1. Robert Arbuckle

    Present address: Present address: Department of Child & Adolescent Psychiatry, School of Medicine, New York University, 550 First Avenue, New York, New York 10016, USA.,

  2. Bao-hua Liu and Guangying K Wu: These authors contributed equally to this work.

Authors and Affiliations

  1. Zilkha Neurogenetic Institute, University of Southern California, 1501 San Pablo Street, Los Angeles, 90033, California, USA

    Bao-hua Liu, Guangying K Wu, Robert Arbuckle, Huizhong W Tao & Li I Zhang

  2. Department of Physiology & Biophysics, University of Southern California, 1501 San Pablo Street, Los Angeles, 90033, California, USA

    Bao-hua Liu & Li I Zhang

  3. Neuroscience Graduate Program, University of Southern California, 1501 San Pablo Street, Los Angeles, 90033, California, USA

    Guangying K Wu

  4. Department of Ophthalmology, Keck School of Medicine, University of Southern California, 1501 San Pablo Street, Los Angeles, 90033, California, USA

    Huizhong W Tao

Authors
  1. Bao-hua Liu
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  3. Robert Arbuckle
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Contributions

L.I.Z. conceived the study. G.K.W. and B.L. carried out the in vivo experiments and data analysis. B.L. modeled the effects of cocktail application on synaptic responses. R.A. was involved in current-clamp recordings. L.I.Z. and H.W.T. supervised the project and wrote the paper.

Corresponding author

Correspondence to Li I Zhang.

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Supplementary Figures 1–7, Table 1 and Notes 1 and 2. (PDF 421 kb)

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Liu, Bh., Wu, G., Arbuckle, R. et al. Defining cortical frequency tuning with recurrent excitatory circuitry. Nat Neurosci 10, 1594–1600 (2007). https://doi.org/10.1038/nn2012

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