Auditory neuroanatomy: the Spanish heritage. Santiago Ramón y Cajal,

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3 Auditory neuroanatomy: the Spanish heritage Santiago Ramón y Cajal, Rafael Lorente de Nó,

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14 The nervous system is made up of cells. Estimates of the number of cells vary from one (the reticular theory) to billions. There are two basic types of cells: nerve cells and glial cells. There is very little extracellular space in the central nervous system.

15 NEURONS To a certain extent, the structure of neurons resembles that of other cells of epithelial origin. There is a cell body containing a nucleus, endoplasmic reticulum, a Golgi apparatus, mitochondria, and so forth. Neurons are specialized for some particular functions. For example, they are responsive to specific forms of energy (which can be mechanical, electromagnetic, thermal, or, as is usually the case in the CNS, chemical). They generate electrical signals or action potentials and transmit them to sites often distant from the cell body. Neurons contact each other at specialized sites known as synapses and through such connections, activity generated in one neuron may cause activity (or inhibit activity) in many others.

16 A typical neuron can be divided into four regions: CELL BODY DENDRITES AXON AXON TERMINALS The cell body contains the nucleus and cytoplasmic machinery for metabolic support of the dendrites and axon. Dendrites are relatively short, branched processes extending from the cell body. They provide extensive surfaces for making contacts with the axon terminals of other nerve cells. Most neurons have multiple dendrites. The axon is a unique process of the cell, usually branched and often quite long. It is specialized for generating action potentials and transmitting them to distant sites. Axon terminals make contact with other nerve cells or with muscles or glands. It is at these terminals that synaptic transmission takes place.

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31 Myelinated axon Synaptic terminal

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34 If you know the answers to these types of questions, you can: Predict and interpret physiological results based on circuitry Make realistic models of neuronal circuits Better understand what goes wrong in disease 34

35 Brainstem auditory pathways: Wiring diagrams and general principles of organization

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40 Descending Commissural Amygdala LPT, PPT

41 Pathways from the cochlear nucleus to the IC can be characterized as direct or indirect Indirect pathways from cochlear nucleus to inferior colliculus via superior olivary complex and nuclei of the lateral lemniscus Direct pathways from cochlear nucleus to inferior colliculus

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43 1. Topographic organization: Mapping of specific features in a systematic manner In the visual system, the visual field is mapped onto the retinal surface. In the somatosensory system, the surface of the body is mapped. In both systems, points that are spatially contiguous are mapped next to each other in the CNS. In the auditory system, the variable that is mapped is FREQUENCY. Auditory space is not mapped at the level of the cochlea. Tonotopic organization of the cat cochlea From Liberman, J. Acoust. Soc. Am., Vol. 72, 1982

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49 Indications of tonotopy and other mapped features are missing from most wiring diagrams

50 2. Identification of subdivisions Almost all auditory areas can be subdivided. It seems likely and in some cases, has been shown that the different subdivisions serve different functions. Subdivision of the IC of the cat based on patterns of Golgi staining From Morest and Oliver, J. Comparative Neurology, 222: , 1984

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56 3. Concept of cell types All auditory areas contain multiple neuronal populations. Each presumably plays a different role in auditory function. Some of the cell types in the cochlear nucleus, defined morphologically

57 The concept of natural cell types... Natural cell types are there to be discovered and demonstrated; they cannot be invented. A type can be equated with a cluster of variables in parametric space. When we say that a cell belongs to a certain cell type, we mean that the cell parameters map to a certain cluster region in parametric space. Each cluster can be labeled categorically, but the label should not be confused with the sum of the variables used to identify the cell type. The more variables that are found to covary, the more certain we can be that we have defined a natural type. As variables are shown to cluster, the claim that the cluster defines a natural cell type should be treated as an hypothesis. From Rodieck and Brening,

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60 Within the serial organization, the ascending auditory system is made up of multiple parallel pathways

61 The specific targets of each identified cell population. The specific cell type that receives the input has been identified in only a few places. Note that the literature review on which this summary is based was completed in It would be a worthwhile exercise to examine the more recent literature looking for additional information about the terminations of each cell type. A good place to start might be Oertel et al., From Cant and Benson,

62 These wiring diagrams illustrate the projection patterns of specific cell types in the cochlear nucleus, but it is almost never possible to illustrate the serial connectivity of specific cell types

63 5. Divergence and convergence of connections a. Some neurons project to multiple targets (divergence). b. Multiple neuronal types may project to the same target (convergence).

64 Convergence of multiple neuronal types onto the same target is of particular interest. For example, we would like to know whether neurons from the cochlear nucleus and superior olivary complex project to the same neurons in the IC or to different sets of neurons.

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69 6. The 6. The auditory auditory system system (like (like other other sensory sensory systems) systems) is made is made up up of both of both ascending ascending and and descending descending pathways. pathways. A complete A complete picture picture of auditory of auditory circuitry circuitry must must include include the the descending descending projections. projections. 69

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71 7. Neuronal response properties depend on a complex interplay of excitatory and inhibitory inputs GAD labeled terminals contacting a cell in the cochlear nucleus From Saint Marie et al., 1989, Hearing Res. 42:97 112

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73 Many wiring diagrams do not include information about the sign of the elements of the circuitry

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75 Inhibitory Excitatory Excitatory

76 8. Specializations of the auditory plan in mammals. Animals evolve to hear the frequencies important for survival in their particular ecological niche. Not all frequencies are equally useful for all mammalian species, and audiograms differ markedly among species. From Koay, Heffner and Heffner, J. Comp. Psychol. 112:

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84 Studies in my lab: I am interested in how cells in different parts of the central nucleus of the inferior colliculus terminate in the medial geniculate nucleus and how these parts of the MG project, in turn, to the auditory cortex. The main methodology is the use of neuroanatomical tracing techniques based on axonal transport. Based on Cant and Benson, 2006 Based on Cant and Benson, 2007 HYPOTHETICAL

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89 I have sometimes heard it said that the nervous system consists of huge numbers of random connections. Although its orderliness is indeed not always obvious, I nevertheless suspect that those who speak of random networks in the nervous system are not constrained by any previous exposure to neuroanatomy. David Hubel Eye, Brain and Vision 89

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91 How do we define neuronal cell types? For many purposes, biologists must study large brains through groups of similar neurons, since these populations not individual cells are the smallest units for which exact counterparts can be recognized unequivocally across a series of brains..... The discovery of neuronal types is best achieved by imitating the naturalist who seeks new biological species: a large sample of cells is gathered by a regular, widely effective method, and an effort is made to understand the biases in the sampling procedure; a numerous and diverse set of features is observed for each neuron encountered; and the cell sets recognized are described in agreement with the polythetic concept of natural groups. The resulting multidimensional population descriptions, the most useful of which include the temporal information available through electrophysiological recording may be quite powerful for testing circuit hypotheses about the large nervous system. C. F. Tyner,

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