Summary
Comparative studies of neural mechanisms underlying the perception of natural stimulus patterns and the control of adaptive behavioral responses have revealed organizational principles that are shared by a wide spectrum of animals. Mechanisms of perception and motor control are commonly executed in a distributed network of neurons that lack ‘pontifical’ elements. Individual neurons even at an organizational level as high as the optic tectum may still have very general response characteristics, and the recruitment of individual neurons reveals little about the nature of the stimulus situation outside. Only the joint evaluation of messages from large populations of such neurons yields unambiguous pictures of the outside world. Stimulus variables are commonly mapped continuously within a stratum of neurons so that their variation over time can be monitored by mechanisms similar to motion detection in a retina. The ordered representation of a stimulus variable within an array of broadly tuned elements allows for a degree of stimulus resolution that by far exceeds that of individual elements in the array. Neural systems are burdened by their evolutionary history and suffer from imperfections that are overcome by a patchwork of compensations. The existence of multiple neuronal representations of sensory information and multiple circuits for the control of behavioral responses should provide the necessary freedom for evolutionary tinkering and the invention of new designs.
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References
Allman JM, Kaas JH (1971) A representation of the visual field in the caudal third of the middle temporal gyrus of the owl monkey (Aotus trivirgatus). Brain Res 31:84–105
Allmann JM, Kaas JH (1974) A crescent-shaped cortical visual area surrounding the middle temporal area (MT) in the owl monkey (Aotus trivirgatus). Brain Res 76:247–265
Allman JM, Baker JF, Newsome WT, Petersen SE (1981) Visual topography and function. In: Woolsey CN (ed) Cortical sensory organization, vol 2. Humana Press, Clifton, New Jersey, pp 171–185
Altes R (1987) Some theoretical concepts for echolocation. In: Nachtigall PE (ed) Proceedings of the 1986 NATO Advanced Study Institute on Animal Sonar Systems. Plenum Press, New York (in press)
Barlow HB (1986) Why have multiple cortical areas? Vision Res 26:81–90
Bell CC (1986) Electroreception in mormyrid fish: Central physiology. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 423–452
Bell CC, Szabo T (1986) Electroreception in mormyrid fish: Central anatomy. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 375–422
Bullock TH, Hamstra RH, Scheich H (1972) The jamming avoidance response of high-frequency electric fish. J Comp Physiol 77:1–48
Calvin WH (1983) A stone's throw and its launch window: Timing precision and its implications for language and hominid brains. J Theor Biol 104:121–135
Carr CE, Maler L (1986) Electroreception in gymnotiform fish: central anatomy and physiology. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 319–374
Carr CE, Heiligenberg W, Rose GJ (1986a) A time-comparison circuit in the electric fish midbrain. I. Behavior and physiology. J Neurosci 6:107–119
Carr CE, Maler L, Taylor B (1986b) A time-comparison circuit in the electric fish midbrain. II. Functional morphology. J Neurosci 6:1372–1383
Dumont PC, Robertson RM (1986) Neuronal circuits: an evolutionary perspective. Science 233:849–853
Eaton RC, Hackett JT (1984) The role of the Mauthner cell in fast starts involving escape in teleost fishes. In: Eaton RC (ed) Neuronal mechanisms of startle behavior. Plenum Press, New York, pp 213–266
Gregory WK (1935) Reduplication in evolution. Q Rev Biol 10:272–290
Griffin DR (1958) Listening in the dark: The acoustic orientation of bats and men. Yale University Press, New Haven, Connecticut
Heiligenberg W (1986) Jamming Avoidance Responses: Model systems for neuroethology. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 613–650
Heiligenberg W, Bastian J (1980) The control ofEigenmannia's pacemaker by distributed evaluation of electroreceptive afferents. J Comp Physiol 136:113–133
Heiligenberg W, Dye J (1982) Labelling of electroreceptive afferents in a gymnotoid fish by intracellular injection of HRP: the mystery of multiple maps. J Comp Physiol 148:287–296
Heiligenberg W, Rose G (1985) Phase and amplitude computations in the midbrain of an electric fish: intracellular studies of neurons participating in the jamming avoidance response (JAR) ofEigenmannia. J Neurosci 5:515–531
Heiligenberg W, Rose GJ (1986) Gating of sensory information: joint computations of phase and amplitude data in the midbrain of the electric fishEigenmannia. J Comp Physiol A 159:311–324
Heiligenberg W, Rose GJ (1987) The optic tectum of the gymnotiform electric fishEigenmannia: labelling of physiologically identified cells. Neuroscience (in press)
Hinton GE, McClelland JL, Rumelhart DE (1986) Distributed representations. In: Rumelhart DE, McCelland JL (eds) Parallel Distributed Processing, vol 1. MIT Press, Cambridge, Massachusetts, pp 77–109
Jacob F (1983) Molecular tinkering in evolution. In: Bendall DS (ed) Evolution from Molecules to Men. Cambridge University Press, pp 132–144
Kawasaki M, Heiligenberg W (1987) Individual prepacemaker neurons can modulate the medullary pacemaker of the gymnotiform electric fish,Eigenmannia. J Comp Physiol (in press)
Konishi M (1986) Centrally synthesized maps of sensory space. TINS 9:163–168
Konishi M, Sullivan EW, Takahashi T (1985) The owl's cochlear nuclei process different sound localization cues. J Acoust Soc Am 78:360–364
Konishi M, Takahashi T, Wagner H, Sullivan WE, Carr CE (1987) Neurophysiological and anatomical substrates of sound localization in the owl. In: Merzenich M, Brugge J (eds) Functions of the auditory system. Neurosciences Institute, New York
Maler L (1976) Two types of laminar neural structure: Examples from weakly electric fish. In: Creutzfeldt O (ed) Afferent and intrinsic organization of laminated structures in the brain. Exp Brain Res [Suppl I]. Springer, Berlin Heidelberg New York, pp 571–579
Merzenich MM, Kaas JH, Sur M, Lin CS (1978) Double representation of the body surface within cytoarchitectonic areas 3b and 1 in ‘SI’ in the owl monkey (Aotus trivirgatus). J Comp Neurol 181:41–74
Neuweiler G (1984) Auditory basis of echolocation in bats. In: Bolis L, Keynes RD, Maddrell SHP (eds) Comparative physiology of sensory systems. Cambridge University Press, pp 115–141
Rose GJ, Heiligenberg W (1986a) Neural coding of difference frequencies in the midbrain of the electric fishEigenmannia: Reading the sense of rotation in an amplitude-phase plane. J Comp Physiol A 158:613–624
Rose GJ, Heiligenberg W (1986b) Limits of phase and amplitude sensitivity in the torus semicircularis ofEigenmannia. J Comp Physiol A 159:813–822
Rose GJ, Keller C, Heiligenberg W (1987) ‘Ancestral’ neural mechanisms of electrolocation suggest a substrate for the evolution of the jamming avoidance response. J Comp Physiol A 160:491–500
Scheich H, Bullock TH, Hamstra RH (1973) Coding properties of two classes of afferent nerve fibers: High-frequency electroreceptors in the electric fishEigenmannia. J Neurophysiol 36:39–60
Schnitzler HU, Menne D, Rudi K, Heblich K (1984) The acoustical image of fluttering insects in echolocating bats. In: Huber F, Markl H (eds) Neuroethology and behavioral physiology. Roots and growing points. Springer, Berlin Heidelberg New York, pp 235–250
Shumway CA (1986) Physiological difference in the multiple maps of the electrosensory lateral line lobe: pyramidal cells have different receptive field sizes. Soc Neurosci Abstr 58.3
Simmons JA (1973) The resolution of target range by echolocating bats. J Acoust Soc 54:157–173
Simmons JA (1979) Perception of echo phase information in bat sonar. Science 204:1336–1338
Strausfeld NJ (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New York
Suga N (1982) Functional organization of the auditory cortex. Representation beyond tonotopy in the bat. In: Woolsey CN (ed) Cortical sensory organization, vol 3. Humana Press, Clifton, New Jersey, pp 157–218
Suga N (1984) The extent to which biosonar information is represented in the bat auditory cortex. In: Edelman GM, Gall WE, Cowan WM (eds) Dynamic aspects of neocortical function. Wiley, New York, pp 315–373
Takahashi T, Moiseff A, Konishi M (1984) Time and intensity cues are processed independently in the auditory system of the owl. J Neurosci 4:1781–1786
Van Essen DC, Maunsell JHR, Bixby JL (1981) Organization of extrastriate visual areas in the Macaque Monkey. In: Woolsey CN (ed) Cortical sensory organization, vol 2. Humana Press, Clifton, New Jersey, pp 157–170
Westheimer G (1981) Visual hyperacuity. Prog Sens Physiol 1:1–30
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Heiligenberg, W. Central processing of sensory information in electric fish. J. Comp. Physiol. 161, 621–631 (1987). https://doi.org/10.1007/BF00603665
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DOI: https://doi.org/10.1007/BF00603665