Abstract
Intrinsic connections in the cat primary auditory field (AI) as revealed by injections Phaseolus vulgaris leucoagglutinin (PHA-L) or biocytin, had an anisotropic and patchy distribution. Neurons, labelled retrogradely with PHA-L were concentrated along a dorsoventral stripe through the injection site and rostral to it; the spread of rostrally located neurons was greater after injections into regions of low rather than high characteristic frequencies. The intensity of retrograde labelling varied from weak and granular to very strong and Golgi-like. Out of 313 Golgi like retrogradely labelled neurons 79.6% were pyramidal, 17.2% multipolar, 2.6% bipolar, and 0.6% bitufted; 13.4% were putatively inhibitory, i.e. aspiny or sparsely spiny multipolar, or bitufted. Individual anterogradely labelled intrinsic axons were reconstructed for distances of 2 to 7 mm. Five main types were distinguished on the basis of the branching pattern and the location of synaptic specialisations. Type 1 axons travelled horizontally within layers II to VI and sent collaterals at regular intervals; boutons were only present in the terminal arborizations of these collaterals. Type 2 axons also travelled horizontally within layers II to VI and had rather short and thin collateral branches; boutons or spine-like protrusions occurred in most parts of the axon. Type 3 axons travelled obliquely through the cortex and formed a single terminal arborization, the only site where boutons were found. Type 4 axons travelled for some distance in layer I; they formed a heterogeneous group as to their collaterals and synaptic specializations. Type 5 axons travelled at the interface between layer VI and the white matter; boutons en passant, spine-like protrusions, and thin short branches with boutons en passant were frequent all along their trajectory. Thus, only some axonal types sustain the patchy pattern of intrinsic connectivity, whereas others are involved in a more diffuse connectivity.
Similar content being viewed by others
Abbreviations
- AAF :
-
anterior auditory cortical field
- AI :
-
primary auditory cortical field
- AII :
-
secondary auditory cortical field
- ALLS :
-
anterolateral lateral suprasylvian visual area
- CF :
-
characteristic frequency
- IFL :
-
isofrequency line
- INJ :
-
injection
- LV :
-
pars lateralis of the ventral division of the MGB
- MGB :
-
medial geniculate body
- mss :
-
middle suprasylvian sulcus
- OV :
-
pars ovoidea of the ventral division of the MGB
- PAF :
-
posterior auditory field
- PHA-L :
-
Phaseolus vulgaris leucoagglutinin
- PO :
-
posterior nucleus of the thalamus
- R :
-
rostral
- SF :
-
suprasylvian fringe
- syl :
-
sylvian sulcus
- TBS :
-
TRIS-buffered saline
- V :
-
ventral
- VL :
-
ventro-lateral nucleus of the MGB
References
Abeles M, Goldstein MH (1970) Functional architecture in cat auditory cortex: columnar organization and organization according to depth. J Neurophysiol 33:172–187
Andersen RA, Knight PL, Merzenich MM (1980) The thalamocortical and corticothalamic connections of AI, AII, the anterior auditory field (AAF) in the cat: evidence for two largely segregated systems of connections. J Comp Neurol 194:663–701
Bolz J, Gilbert CD, Wiesel TN (1989) Pharmacological analysis of cortical circuitry. Trends Neurosci 12:292–296
Brandner S, Redies H (1990) The projection from medial geniculate body to field AI in cat: organization in the isofrequency dimension. J Neurosci 10:50–61
Castel M, Spira ME, Parnas I, Yarom Y (1976) Ultrastructure of region of a low safety factor in inhomogeneous giant axon of the cockroach. J Neurophysiol 39:900–907
Chung S-H, Raymond SA, Lettvin JY (1970) Multiple meaning in single visual units. Brain Behav Evol 3:72–101
Clarke S, Innocenti GM (1990) Auditory neurons with transitory axons to visual areas form short permanent projections. Eur J Neurosci 2:227–242
Clarke S, de Ribaupierre F (1992) Intrinsic connections at the boundaries of the primary auditory cortex (AI) (abstract). Experientia 48:A87
Clarke S, Rouiller EM, de Ribaupierre F (1990) Morphology of intrinsic axons in auditory cortical field AI (abstract). Eur J Neurosci [Suppl 13]: 155
Clarke S, de Ribaupierre F, Rouiller EM (1991) Connections with the cat primary auditory cortex as revealed by retrograde transport of PHA-L (abstract). Eur J Neurosci [Suppl 14]:41
Cliffer KD, Giesler GJ Jr (1988) PHA-L can be transported anterogradely through fibers of passage. Brain Res 458:185–191
Dickson JW, Gerstein GL (1974) Interactions between neurons in the auditory cortex of cat. J Neurophysiol 37:1239–1261
Eckhorn R, Bauer R, Jordan W, Brosch M, Kruse W, Munk M, Reitboeck HJ (1988) Coherent oscillations: a mechanism of feature linking in the visual cortex? Biol Cybern 60:121–130
Eysel UT, Wörgötter F, Pape HC (1987) Local cortical lesions abolish lateral inhibition at direction-selective cells in cat visual cortex. Exp Brain Res 68:606–612
Eysel UT, Muche T, Wörgötter F (1988) Lateral interactions at direction-selective striate neurones in the cat demonstrated by local cortical inactivation. J Physiol 399:657–675
Fairén A, DeFelipe J, Regidor J (1984) Nonpyramidal neurons. In: Peters A, Jones EG (eds) Cerebral cortex, vol 1. Cellular components of the cerebral cortex. Plenum Press, New York London, pp 201–253
Feldman ML (1984) Morphology of the neocortical pyramidal neuron. In: Peters A, Jones EG (eds) Cerebral cortex, vol 1. Cellular components of the cerebral cortex. Plenum Press, New York London, pp 123–200
Gerfen CR, Sawchenko P (1985) A method for anterograde axonal tracing of chemically specified circuits in the CNS: a combined Phaseolus Vulgaris-Leucoagglutinin (PHA-L) tract tracing and immunohistochemistry. Brain Res 343:144–150
Gerfen CR, Sawchenko PE (1984) An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons, and terminals: immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris Leucoagglutinin (PHA-L). Brain Res 290:219–238
Gilbert CD, Wiesel TN (1979) Morphology and intracortical projections of functionally characterized neurones in the cat visual cortex. Nature 280:120–125
Gilbert CD, Wiesel TN (1983) Clustered intrinsic connections in cat visual cortex. J Neurosci 3:1116–1133
Gilbert CD, Wiesel TN (1989) Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex. J Neurosci 9:2432–2442
Gray CM, Singer W (1989) Stimulus-specific neuronal oscillations of orientation columns of cat visual cortex. Proc Natl Acad Sci USA 86:1698–1702
Groenewegen HJ, Wouterlood FG (1990) Light and electron microscopic tracing of neuronal connections with Phaseolus vulgaris-leucoagglutinin (PHA-L), combinations with other neuroanatomical techniques. In: Björklund A, Hökfelt T, Wouterlood FG, Van den Pol AN (eds) Handbook of Chemical Neuroanatomy. Elsevier Science, New York pp 47–124
Grossman Y, Spira ME, Parnas I (1973) Differential flow of information into branches of a single axon. Brain Res 64:379–386
Heil P, Rajan R, Irvine DRF (1992) Sensitivity of neurons in cat primary auditory cortex to tones and frequency-modulated stimuli. II. Organization of response porperties along the “isofrequency” dimension. Hear Res 63:135–156
Imig TJ, Adrian HO (1977) Binaural columns in the primary field (AI) of cat auditory cortex. Brain Res 138:241–257
Imig TJ, Brugge JF (1978) Sources and terminations of callosal axons related to binaural and frequency maps in primary auditory cortex of the cat. J Comp Neurol 182:637–660
Imig TJ, Morel A (1983) Organization of the thalamocortical auditory system in the cat. Ann Rev Neurosci 6:95–120
Imig TJ, Morel A (1984) Topographic and cytoarchitectonic organization of thalamic neurons related to their targets in low-, medium-, and high-frequency representations in cat auditory cortex. J Comp Neurol 227:511–539
Imig TJ, Reale RA (1980) Patterns of cortico-cortical connections related to tonotopic maps in cat auditory cortex. J Comp Neurol 192:293–332
Imig TJ, Reale RA (1981) Ipsilateral cortico-cortical projections related to binaural columns in cat primary auditory cortex. J Comp Neurol 203:1–14
Jones EG, Hendry SHC (1984) Basket cells. In: Peters A, Jones EG (eds) Cerebral cortex, vol 1. Cellular components of the cerebral cortex. Plenum Press, New York London, pp 309–336
Kisvarday ZF, Eysel UT (1992) Cellular organization of reciprocal patchy networks in layer III of cat visual cortex (area 17). Neuroscience 46:275–286
Kisvarday ZF, Martin KAC, Friedlander MJ, Somogyi P (1987) Evidence for interlaminar inhibitory circuits in the striate cortex of the cat. J Comp Neurol 260:1–19
King MA, Louis PA, Hunter BE, Walker DW (1989) Biocitin: a versatile anterograde neuroanatomical tract-tracing alternative. Brain Res 497:361–367
Kita H, Kitai ST (1987) Efferent projections of the subthalamic nucleus in the rat: light and electron microscopic analysis with the PHA-L method. J Comp Neurol 260:435–452
LeVay S (1988) Patchy intrinsic projections in visual cortex, area 18, of the cat: morphological and immunocytochemical evidence for an excitatory function. J Comp Neurol 269:265–274
Lund JS, Henry GH, MacQueen CL, Harvey AR (1979) Anatomical organisation of the primary visual cortex (area 17) of the cat: a comparison with area 17 of the macaque monkey. J Comp Neurol 184:599–618
Martin KAC (1984) Neuronal circuits in cat striate cortex. In: Jones EG, Peters A (eds) Cerebral cortex, vol 2. Functional properties of cortical cells. Plenum Press, New York London, pp 241–284
Martin KAC, Whitteridge D (1984) Form, function and intracortical projections of spiny neurones in the striate visual cortex of the cat. J Physiol 353:463–504
Matsubara JA, Phillips DP (1988) Intracortical connections and their physiological correlates in the primary auditory cortex (AI) of the cat. J Comp Neurol 268:38–48
Matsubara JA, Cynader MS, Swindale NV (1987) Anatomical properties and physiological correlates of the intrinsic connections in cat area 18. J Neurosci 7:1428–1446
McMullen NT, Glaser EM (1982) Tonotopic organization of rabbit auditory cortex. Exp Neurol 75:208–220
Merzenich MM, Knight PL, Roth GL (1975) Representation of cochlea within primary auditory cortex in the cat. J Neurophysiol 38:231–249
Middlebrooks JC, Zook JM (1983) Intrinsic organization of the cat's medial geniculate body identified by projections to binaural response-specific bands in the primary auditory cortex. J Neurosci 3:203–224
Middlebrooks JC, Dikes RW, Merzenich MM (1980) Binaural response-specific bands in primary auditory cortex (AI) of the cat: topographical organization orthogonal to isofrequency contours. Brain Res 181:31–48
Mitani A, Shimokouchi M, Itoh K, Nomura S, Kudo M, Mizuno N (1985) Morphology and laminar organization of electrophysiologically identified neurons in the primary auditory cortex in the cat. J Comp Neurol 235:430–447
Mitchison G, Crick F (1982) Long axons within the striate cortex: their distribution, orientation and patterns of connection. Proc Natl Acad Sci USA 79:3661–3665
Morel A, Imig TJ (1987) Thalamic projections to fields A, AI, P, and VP in the cat auditory cortex. J Comp Neurol 265:119–144
Murakami F, Song W-J (1988) Climbing fibers are labelled after injection of PHA-L into the nucleus interpositus of the cat. Brain Res 463:144–147
Ojima H, Honda CN, Jones EG (1991) Patterns of axon collateralization of identified supragranular pyramidal neurons in the cat auditory cortex. Cerebral Cortex 1:80–94
Ojima H, Honda CN, Jones EG (1992) Characteristics of intracellularly injected infragranular pyramidal neurons in cat primary auditory cortex. Cerebral Cortex 2:197–216
Palmer LA, Rosenquist AC, Tusa RJ (1978) The retinotopic organization of lateral suprasylvian visual areas in the cat. J Comp Neurol 177:237–256
Parnas I (1972) Differential block at high frequency of branches of a single axon innervating two muscles. J Neurophysiol 35:903–914
Peters A (1984) Bipolar cells. In: Peters A, Jones EG (eds) Cerebral cortex, vol 1. Cellular components of the cerebral cortex. Plenum Press, New York London, pp 381–407
Peters A, Jones EG (1984) Classification of cortical neurons. In: Peters A, Jones EG (eds) Cerebral cortex, vol 1. Cellular components of the cerebral cortex. Plenum Press, New York London, pp 107–121
Phillips DP, Irvine DRF (1981) Responses of single neurons in physiologically defined area AI of cat cerebral cortex: sensitivity to interaural intensity difference. Hearing Res 4:299–307
Rajan R, Aitkin LM, Irvine DRF, McKay J (1990) Azimuthal sensitivity of neurons in primary auditory cortex of cats. I. Types of sensitivity and the effects of variations in stimulus parameters. J Neurophysiol 64:872–887
Reale RA, Imig TJ (1980) Tonotopic organization of auditory cortex in the cat. J Comp Neurol 192:265–291
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
de Ribaupierre F, Abeles M, de Ribaupierre Y (1985) Influence of tangential cortical distance on single unit interactions in the cat auditory cortex (abstract). Neurosci Lett [Suppl 22]:S433
Rouiller EM, de Ribaupierre F (1990) Arborization of corticothalamic axons in the auditory thalamus of the cat: a PHA-L tracing study. Neurosci Lett 108:29–35
Rouiller EM, Rodrigues-Dagaeff C, Simm D, de Ribaupierre Y, Villa A, de Ribaupierre Y (1989) Functional organization of the medial division of the medial geniculate body of cat: tonotopic organization, spatial distribution of response properties and cortical connections. Hearing Res 39:127–142
Rouiller EM, Simm GM, Villa AEP, de Ribaupierre Y, de Ribaupierre F (1991) Auditory corticocortical interconnections in the cat: Evidence for parallel and hierarchical arrangement of the auditory cortical areas. Exp Brain Res 86:483–505
Schofield BR (1990) Uptake of Phaseolus vulgaris leucoagglutinin (PHA-L) by axons of passage. J Neurosci Methods 35:47–56
Schreiner CE, Mendelson JR (1990) Functional topography of cat primary auditory cortex: distribution of integrated excitation. J Neurophysiol 64:1442–1459
Schwark HD, Jones EG (1989) The distribution of intrinsic cortical axons in area 3b of cat primary somatosensory cortex. Exp Brain Res 78:501–513
Shu SY, Peterson GM (1988) Anterograde and retrograde axonal transport of Phaseolus vulgaris leucoagglutinin (PHA-L) from the globus pallidus to the striatum of the rat. J Neurosci Methods 25:175–180
Simm G (1991) Etude des propriétés fonctionnelles des aires corticales auditives et de leurs interactions chez le chat. Thesis, University of Lausanne
Somogyi P (1986) Seven distinct types of GABA-immunoreactive neurons in the visual cortex of cat (abstract). Soc Neurosci Abs 12:583
Spira ME, Yarom Y, Parnas I (1976) Modulation of spike frequency by regions of special axonal geometry and by synaptic inputs. J Neurophysiol 39:882–899
Stockbridge N, Stockbridge LL (1988) Differential conduction at axonal bifurcations I. Effect of electrotonic length. J Neurophysiol 59:1277–1285
Van Essen DC (1973) The contribution of membrane hyperpolarization to adaptation and conduction block in sensory neurones of the leech. J Physiol 230:509–534
Wallace MN, Kitzes LM, Jones EG (1991) Intrinsic inter- and intralaminar connections and their relationship to the tonotopic map in cat primary auditory cortex. Exp Brain Res 86:527–544
Winer JA (1984a) Anatomy of layer IV in cat primary auditory cortex (A1). J Comp Neurol 224:535–567
Winer JA (1984b) The non-pyramidal cells in layer III of cat primary auditory cortex. J Comp Neurol 229:512–530
Winer JA (1985) Structure of layer II in cat primary auditory cortex (AI). J Comp Neurol 238:10–37
Winer JA (1992) The functional architecture of the medial geniculate body and of the primary auditory cortex. In: Webster DB, Popper AN, Fay RR (eds) The mammalian auditory pathway: neuroanatomy. Springer, Berlin Heidelberg New York, pp 223–409
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Clarke, S., de Ribaupierre, F., Rouiller, E.M. et al. Several neuronal and axonal types form long intrinsic connections in the cat primary auditory cortical field (AI). Anat Embryol 188, 117–138 (1993). https://doi.org/10.1007/BF00186246
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00186246