Skip to main content
Log in

A computational framework for topographies of cortical areas

  • Original Paper
  • Published:
Biological Cybernetics Aims and scope Submit manuscript

Abstract

Self-organizing feature maps (SOFMs) represent a dimensionality-reduction algorithm that has been used to replicate feature topographies observed experimentally in primary visual cortex (V1). We used the SOFM algorithm to model possible topographies of generic sensory cortical areas containing up to five arbitrary physiological features. This study explored the conditions under which these multi-feature SOFMs contained two features that were mapped monotonically and aligned orthogonally with one another (i.e., “globally orthogonal”, as well as the conditions under which the map of one feature aligned with the longest anatomical dimension of the modeled cortical area (i.e., “dominant”. In a single SOFM with more than two features, we never observed more than one dominant feature, nor did we observe two globally orthogonal features in the same map in which a dominant feature occurred. Whether dominance or global orthogonality occurred depended upon how heavily weighted the features were relative to one another. The most heavily weighted features are likely to correspond to those physical stimulus properties transduced directly by the sensory epithelium of a particular sensory modality. Our results imply, therefore, that in the primary cortical area of sensory modalities with a two-dimensional sensory epithelium, these two features are likely to be organized globally orthogonally to one another, and neither feature is likely to be dominant. In the primary cortical area of sensory modalities with a one-dimensional sensory epithelium, however, this feature is likely to be dominant, and no two features are likely to be organized globally orthogonally to one another. Because the auditory system transduces a single stimulus feature (i.e., frequency) along the entire length of the cochlea, these findings may have particular relevance for topographic maps of primary auditory cortex.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Blasdel GG, Salama G (1986) Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature 321: 579–585

    Article  CAS  PubMed  Google Scholar 

  • Cheung S, Bedenbaugh P, Nagarajan S, Schreiner C (2001) Functional organization of squirrel monkey primary auditory cortex: responses to pure tones. J Neurophysiol 85: 1732–1749

    CAS  PubMed  Google Scholar 

  • Clarey JC, Barone P, Imig TJ (1994) Functional organization of sound direction and sound pressure level in primary auditory cortex of the cat. J Neurophysiol 72: 2383–2405

    CAS  PubMed  Google Scholar 

  • Erwin E, Obermayer K, Schulten K (1995) Models of orientation and ocular dominance columns in the visual cortex: a critical comparison. Neural Comput 7: 425–468

    Article  CAS  PubMed  Google Scholar 

  • Esser KH, Eiermann A (1999) Tonotopic organization and parcellation of auditory cortex in the FM-bat Carollia perspicillata. Eur J Neurosci 11: 3669–3682

    Article  CAS  PubMed  Google Scholar 

  • Farley BJ, Yu H, Jin DZ, Sur M (2007) Alteration of visual input results in a coordinated reorganization of multiple visual cortex maps. J Neurosci 27: 10299–10310

    Article  CAS  PubMed  Google Scholar 

  • Godey B, Atencio CA, Bonham BH, Schreiner CE, Cheung SW (2005) Functional organization of squirrel monkey primary auditory cortex: responses to frequency-modulation sweeps. J Neurophysiol 94: 1299–1311

    Article  PubMed  Google Scholar 

  • Imig TJ, Adrian HO (1977) Binaural columns in the primary field (A1) of cat auditory cortex. Brain Res 138: 241–257

    Article  CAS  PubMed  Google Scholar 

  • Kelly JB, Judge PW (1994) Binaural organization of primary auditory cortex in the ferret (Mustela putorius). J Neurophysiol 71: 904–913

    CAS  PubMed  Google Scholar 

  • Kilgard MP, Merzenich MM (1998) Cortical map reorganization enabled by nucleus basalis activity. Science 279: 1714–1718

    Article  CAS  PubMed  Google Scholar 

  • Kilgard MP, Pandya PK, Vazquez J, Gehi A, Schreiner CE, Merzenich MM (2001) Sensory input directs spatial and temporal plasticity in primary auditory cortex. J Neurophysiol 86: 326–338

    CAS  PubMed  Google Scholar 

  • Kohonen T (1990) The self-organizing map. Proc IEEE 78: 1464–1480

    Article  Google Scholar 

  • Koulakov AA, Chklovskii DB (2001) Orientation preference patterns in mammalian visual cortex: a wire length minimization approach. Neuron 29: 519–527

    Article  CAS  PubMed  Google Scholar 

  • Langner G, Sams M, Heil P, Schulze H (1997) Frequency and periodicity are represented in orthogonal maps in the human auditory cortex: evidence from magnetoencephalography. J Comp Physiol [A] 181: 665–676

    Article  CAS  Google Scholar 

  • Matsubara J, Phillips D (1988) Intracortical connections and their physiological correlates in the primary auditory cortex (AI) of the cat. J Comp Neurol 268: 38–48

    Article  CAS  PubMed  Google Scholar 

  • Mendelson JR, Schreiner CE, Sutter ML (1997) Functional topography of cat primary auditory cortex: response latencies. J Comp Physiol [A] 181: 615–633

    Article  CAS  Google Scholar 

  • Mendelson JR, Schreiner CE, Sutter ML, Grasse KL (1993) Functional topography of cat primary auditory cortex: responses to frequency-modulated sweeps. Exp Brain Res 94: 65–87

    Article  CAS  PubMed  Google Scholar 

  • Merzenich MM, Knight PL, Roth GL (1973) Cochleotopic organization of primary auditory cortex in the cat. Brain Res 63: 343–346

    Article  CAS  PubMed  Google Scholar 

  • Merzenich MM, Knight PL, Roth GL (1975) Representation of cochlea within primary auditory cortex in the cat. J Neurophysiol 38: 231–249

    CAS  PubMed  Google Scholar 

  • Middlebrooks JC, Xu L, Eddins AC, Green DM (1998) Codes for sound-source location in nontonotopic auditory cortex. J Neurophysiol 80: 863–881

    CAS  PubMed  Google Scholar 

  • Mountcastle VB (1997) The columnar organization of the neocortex. Brain 120(Pt 4): 701–722

    Article  PubMed  Google Scholar 

  • Obermayer K, Blasdel GG, Schulten K (1992) Statistical-mechanical analysis of self-organization and pattern formation during the development of visual maps. Phys Rev A 45: 7568–7589

    Article  PubMed  Google Scholar 

  • Ojima H, Takayanagi M (2004) Cortical convergence from different frequency domains in the cat primary auditory cortex. Neuroscience 126: 203–212

    Article  CAS  PubMed  Google Scholar 

  • Ojima H, Takayanagi M, Potapov D, Homma R (2005) Isofrequency band-like zones of activation revealed by optical imaging of intrinsic signals in the cat primary auditory cortex. Cereb Cortex 15: 1497–1509

    Article  CAS  PubMed  Google Scholar 

  • Philibert B, Beitel RE, Nagarajan SS, Bonham BH, Schreiner CE, Cheung SW (2005) Functional organization and hemispheric comparison of primary auditory cortex in the common marmoset (Callithrix jacchus). J Comp Neurol 487: 391–406

    Article  PubMed  Google Scholar 

  • Read HL, Winer JA, Schreiner CE (2001) Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex. Proc Natl Acad Sci USA 98: 8042–8047

    Article  CAS  PubMed  Google Scholar 

  • Read HL, Winer JA, Schreiner CE (2002) Functional architecture of auditory cortex. Curr Opin Neurobiol 12: 433–440

    Article  CAS  PubMed  Google Scholar 

  • Reale RA, Brugge JF, Feng JZ (1983) Geometry and orientation of neuronal processes in cat primary auditory cortex (AI) related to characteristic-frequency maps. Proc Natl Acad Sci USA 80: 5449–5453

    Article  CAS  PubMed  Google Scholar 

  • Recanzone GH, Schreiner CE, Sutter ML, Beitel RE, Merzenich MM (1999) Functional organization of spectral receptive fields in the primary auditory cortex of the owl monkey. J Comp Neurol 415: 460–481

    Article  CAS  PubMed  Google Scholar 

  • Ritter H, Schulten K (1988) Convergence properties of Kohonen’s topology conserving maps: fluctuations, stability, and dimension selection. Biol Cybern 60: 59–71

    Article  Google Scholar 

  • Rutkowski RG, Wallace MN, Shackleton TM, Palmer AR (2000) Organisation of binaural interactions in the primary and dorsocaudal fields of the guinea pig auditory cortex. Hear Res 145: 177–189

    Article  CAS  PubMed  Google Scholar 

  • Schreiner CE (1995) Order and disorder in auditory cortical maps. Curr Opin Neurobiol 5: 489–496

    Article  CAS  PubMed  Google Scholar 

  • Schreiner CE, Mendelson JR (1990) Functional topography of cat primary auditory cortex: distribution of integrated excitation. J Neurophysiol 64: 1442–1459

    CAS  PubMed  Google Scholar 

  • Schreiner CE, Mendelson JR, Sutter ML (1992) Functional topography of cat primary auditory cortex: representation of tone intensity. Exp Brain Res 92: 105–122

    Article  CAS  PubMed  Google Scholar 

  • Schulze H, Langner G (1997a) Periodicity coding in the primary auditory cortex of the Mongolian gerbil (Meriones unguiculatus): two different coding strategies for pitch and rhythm. J Comp Physiol [A] 181: 651–663

    Article  CAS  Google Scholar 

  • Schulze H, Langner G (1997b) Representation of periodicity pitch in the primary auditory cortex of the Mongolian gerbil. Acta Otolaryngol Suppl 532: 89–95

    Article  CAS  PubMed  Google Scholar 

  • Shamma SA, Fleshman JW, Wiser PR, Versnel H (1993) Organization of response areas in ferret primary auditory cortex. J Neurophysiol 69: 367–383

    CAS  PubMed  Google Scholar 

  • Swindale NV (1991) Coverage and the design of striate cortex. Biol Cybern 65: 415–424

    Article  CAS  PubMed  Google Scholar 

  • Swindale NV (2004) How different feature spaces may be represented in cortical maps. Network 15: 217–242

    Article  CAS  PubMed  Google Scholar 

  • Swindale NV, Shoham D, Grinvald A, Bonhoeffer T, Hubener M (2000) Visual cortex maps are optimized for uniform coverage. Nat Neurosci 3: 822–826

    Article  CAS  PubMed  Google Scholar 

  • Tootell RB, Hamilton SL, Silverman MS, Switkes E (1988a) Functional anatomy of macaque striate cortex. I. Ocular dominance, binocular interactions, and baseline conditions. J Neurosci 8: 1500–1530

    CAS  PubMed  Google Scholar 

  • Tootell RB, Silverman MS, Hamilton SL, De Valois RL, Switkes E (1988b) Functional anatomy of macaque striate cortex. III. Color. J Neurosci 8: 1569–1593

    CAS  PubMed  Google Scholar 

  • Tootell RB, Silverman MS, Hamilton SL, Switkes E, De Valois RL (1988c) Functional anatomy of macaque striate cortex. V. Spatial frequency. J Neurosci 8: 1610–1624

    CAS  PubMed  Google Scholar 

  • Tootell RB, Switkes E, Silverman MS, Hamilton SL (1988d) Functional anatomy of macaque striate cortex. II. Retinotopic organization. J Neurosci 8: 1531–1568

    CAS  PubMed  Google Scholar 

  • Ts’o D, Gilbert C, Wiesel T (1986) Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis. J Neurosci 6: 1160

    PubMed  Google Scholar 

  • Watkins PV, Barbour DL (2005) Computational topographies of auditory cortex. In: Society for neuroscience abstracts, Washington, DC

  • Yu H, Farley BJ, Jin DZ, Sur M (2005) The coordinated mapping of visual space and response features in visual cortex. Neuron 47: 267–280

    Article  CAS  PubMed  Google Scholar 

  • Zhang LI, Bao S, Merzenich MM (2001) Persistent and specific influences of early acoustic environments on primary auditory cortex. Nat Neurosci 4: 1123–1130

    Article  CAS  PubMed  Google Scholar 

  • Zhang LI, Tan AY, Schreiner CE, Merzenich MM (2003) Topography and synaptic shaping of direction selectivity in primary auditory cortex. Nature 424: 201–205

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Dyck RH, Hamilton SE, Nathanson NM, Yan J (2005) Disrupted tonotopy of the auditory cortex in mice lacking M1 muscarinic acetylcholine receptor. Hear Res 201: 145–155

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dennis L. Barbour.

Additional information

This research was supported by The McDonnell Center for Higher Brain Function, The Wallace H. Coulter Foundation and NIH grant DC008880.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Watkins, P.V., Chen, T.L. & Barbour, D.L. A computational framework for topographies of cortical areas. Biol Cybern 100, 231–248 (2009). https://doi.org/10.1007/s00422-009-0294-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00422-009-0294-9

Keywords

Navigation