Receptive-field construction in cortical inhibitory interneurons – documents.tips anoxia definicion

Receptive-field

Construction in cortical

Inhibitory interneurons

Harvey A. Swadlow1 and alexander G. Gusev1,2

1 department of psychology, the university of connecticut, 406 babbidge road,

Storrs, connecticut 06269, USA

2 moscow brain research institute, russian academy of medical sciences, per.

Obukha 5, moscow 103064, russia

Correspondence should be addressed to H.A.S. (swadlow@psych.Psy.Uconn.Edu)

Published online: 22 april 2002, DOI: 10.1038/nn847

In the somatosensory âbarrelâ cortex1 (where each barrel repre-

Sents an individual whisker) the receptive fields of cortical spiny

Neurons show considerable specificity for the direction of whisker


Displacement, as do the receptive fields of thalamocortical (TC)

anoxia definicion

Neurons that provide input to the barrels. In contrast, putative

Fast-spike inhibitory interneurons in layer 4 of the barrel cortex

Lack directional preference, but are exquisitely sensitive to low

Stimulus intensities2,3. Here we show, in adult rabbits, that these

Sensitive and broadly tuned inhibitory receptive fields are gen-

Erated by an unselective pooling of convergent functional inputs

From topographically aligned TC neurons with very diverse

Response properties.

A large gap in our understanding of sensory neocortex con-

Cerns the functional properties of inhibitory interneurons and the

Circuitry through which these properties are synthesized. Feed-

Forward inhibition is thought to shape the receptive fields of sen-

anoxia definicion

Sory cortical neurons by suppressing responses to non-optimal

Stimuli4â7. This may be mediated by interneurons with sensitive

And broadly-tuned receptive fields that maintain sharp tuning in

Cortical target neurons in the face of increasing stimulus intensi-

Ty4. Here, we tested a proposal8 that these properties, as found in

Layer-4 inhibitory interneurons of somatosensory cortex (S1), are

Synthesized from a highly convergent/divergent functional TC

Input. In fully awake dutch-belted rabbits, we simultaneously

Recorded from several TC neurons and from several cortical

Interneurons in the S1 barrel that receives these TC inputs (name-

Ly, the barrel with sensory receptive fields that are topographically

anoxia definicion

Aligned with those of the TC neurons). We then examined func-

Tional connectivity using cross-correlation methods. (for experi-

Mental details, see supplementary methods online; experimental

Protocols were approved by the university of connecticut insti-

Tutional animal care and use committee.)

Each TC neuron studied had a receptive field that was domi-

Nated by a single vibrissa (whisker) and an axon that projected

To the S1 barrel under study (shown by spike-triggered averag-

Ing7). Suspected inhibitory interneurons (sins) were identified by

A high-frequency (600 hz) burst of three or more spikes in

Response to thalamic stimulation, and by short spike durations3.

All sins studied responded to peripheral stimulation (air-puff)

anoxia definicion

Of their principal vibrissa at latencies indicative of monosynaptic

TC activation (

Each SIN) and with their broad directional tuning3. In feline

Visual cortex, interneurons with such properties could mediate

The contrast-invariant orientation tuning seen in many cortical

Neurons4. In rabbit or rodent S1, such interneurons may, in a

Similar manner, enhance directional tuning and may constrain

The spatial extent of the receptive field. The present results sup-

Port the notion that sins obtain their receptive field properties

By pooling the inputs from TC neurons that display a wide vari-

Ety of response properties8. Recent findings of electrical coupling

Among cortical fast-spike interneurons12,13 indicate that these

anoxia definicion

Interneurons may be functionally linked by both divergent TC

Axons and electrically coupled dendrites. These mechanisms

Could act synergistically to facilitate widespread, synchronous

Discharge of fast-spike interneurons following TC impulses.

These network characteristics, combined with the extensive local

Axonal arborization of nonspiny interneurons in S1 barrels14,

Are well-suited to mediate a fast, synchronous15 and highly sen-

Sitive feed-forward inhibition of cortical target neurons, per-

Mitting spike generation following only the most optimal

Feed-forward excitatory inputs4â7.

Note: supplementary information is available on the nature neuroscience website.

Acknowledgments

We thank K. Lukatela and J.-M.Anoxia definicion alonso for comments and discussions.

Supported by grants from the national institutes of mental health (MH-

64024), the national science foundation (IBN-0077694) and the russian

Foundation of basic research (00-04-49163).

Competing interests statement

The authors declare that they have no competing financial interests.

RECEIVED 27 NOVEMBER 2001; ACCEPTED 26 FEBRUARY 2002

1. Woolsey, T. Van der loos, H. Brain res. 17, 205â242 (1970).

2. Simons, D. J. Carvell, G. J. Neurophysiol. 61, 311â320 (1989).

3. Swadlow, H. A. J. Neurophysiol. 62, 288â308 (1989).

4. Troyer, T. W., krukowski, A. E., priebe, N. J. Miller, K. D. J. Neurosci. 18,

5908â5927 (1998).

5. Krukowski, A. E. Miller, K. D. Nat. Neurosci. 4, 424â430 (2001).Anoxia definicion

6. Miller, K. D., pinto, D. J. Simons, D. J. Curr. Opin. Neurobiol. 488â497

(2001).

7. Swadlow, H. A. Gusev, A. G. J. Neurophysiol. 83, 2803â2813 (2000).

8. Swadlow, H. A. J. Neurophysiol. 73, 1584â1599 (1995).

9. Reid, R. C. Alonso, J. M. Nature 378, 281â284 (1995).

10. Alonso, J. M., usrey, W. M. Reid, R. C. J. Neurosci. 21, 4001â4015 (2001).

11. Miller, L. M., escabi, M., read, H. L. Schreiner, C. E. Neuron 32, 151â160

(2001).

12. Gibson, J. R., beierlein, M. Connors, B. W. Nature 402, 75â79 (1999).

13. Galarreta, M. Hestrin, S. Nature 402, 72â75 (1999).

14. Woolsey, T. A. Harris, R. M. J. Comp. Neurol. 220, 63â79 (1983).

15. Swadlow, H. A., beloozerova, I. Sirota, M. J. Neurophysiol. 79, 567â582

anoxia definicion

(1998).

Fig. 2. A powerful case of TC divergence: TC neuron âherculesâ stud-

Ied with nine different sins (1â9) during four recording sessions.

(a) auto-correlograms of hercules, obtained during the four record-

Ing sessions when the indicated sins were studied (y-axis values are in

Spikes/s). (b, c) functional connectivity between hercules and sins (b)

And associated cross-correlograms (c; y-axis values are in spikes/s).

Although the efficacy of the functional contacts varied considerably,

Each correlogram showed a significant (P 0.005) peak in spike fre-

Quency at intervals of 1.2â1.9 ms after TC spikes. (d) efficacy values for

TC contacts made by hercules (black), and for other tcâsin pairs

That either reached statistical significance (P 0.005; striped bars) or

anoxia definicion

Did not (open bar). Y-axis values are in spikes/s.

404 nature neuroscience ⢠volume 5 no 5 ⢠may 2002

Brief communications

Contacts made by hercules with each of the sins studied

(fig. 2b), and associated cross-correlograms (fig. 2c). Each cor-

Relogram showed a significant (P 0.005) peak in SIN spike fre-

Quency at intervals of 1.2â1.9 ms following the TC spike. Efficacy

Values for all TC-SIN pairs studied (fig. 2d) show that hercules

Was responsible for the three strongest TC contacts made (with

SINs 4, 6 and 7). The median efficacy of this TC neuron with the

Nine sins was 0.048, which was significantly higher than values

Generated by the other 27 TC neurons (median, 0.012; mann-

Whitney U-test, P = 0.0002).Anoxia definicion this indicates that some TC neu-

Rons, such as hercules, are far more effective than others in

Activating neurons in their targeted cortical column.

There is considerable evidence that receptive fields of first-

Order excitatory neurons in layer 4 of visual and auditory cortex

Are generated by a highly selective convergence of TC inputs9â11.

We do not yet know how the receptive fields of spiny (excitatory)

Neurons in rabbit or rodent barrel cortex are synthesized, but as

Most are well tuned to stimulus direction2,3, they probably receive

Selective input from similarly tuned TC neurons. By contrast, a

Very different model for receptive field construction in feed-

Forward inhibitory interneurons emerges from our results.Anoxia definicion we

Show that an unselective, highly divergent and convergent func-

Tional network links TC neurons with fast-spike cortical interneu-

Rons. No evidence of specificity was seen in the functional

Connectivity between TC neurons and targeted sins, other than

The requirement for precise topographic alignment. Instead, TC

Neurons with very different preferred stimulus directions func-

Tionally target the same cortical SIN.

This high degree of convergence and lack of specificity in TC

Connectivity is consistent with the extremely low thresholds of sins

To sensory stimulation (because many TC neurons may activate

A b c

D

©

20

02

N

At

Ur

E

Pu

Bl

Is

Hi

Ng

G

Ro

U

P

H

Ttp

://

Ne

Ur

O

Sc

I.N

At

Ur

E.

Co

M

1 nature neuroscience ⢠volume 5 no 7 ⢠july 2002

anoxia definicion

Errata

Receptive-field construction in cortical inhibitory interneurons

Harvey A. Swadlow alexander G. Gusev

Nat. Neurosci. 5, 403â404 (2002)

We introduced an error in preparing this article for press. The fifth sentence of the fourth paragraph, ânotably, each of the TC neu-

Rons showed strong directional selectivity, but these preferred directions differed over a range of 13°,â should have read âover a range

Of 135°.Â

©

20

02

N

At

Ur

E

Pu

Bl

Is

Hi

Ng

G

Ro

U

P

H

Ttp

://

Ne

Ur

O

Sc

I.N

At

Ur

E.

Co

M