Abstract
Projections from the auditory thalamus to the amygdala have been implicated in the processing of the emotional signficance of auditory stimuli. In order to further our understanding of the contribution of thalamoamygdala projections to auditory emotional processing, acoustic response properties of single neurons were examined in the auditory thalamus of chloral hydrate-anesthetized rats. The emphasis was on the medial division of the medial geniculate body (MGm), the suprageniculate nucleus (SG), and the posterior intralaminar nucleus (PIN), thalamic areas that receive inputs from the inferior colliculus and project to the lateral nucleus of the amygdala (AL). For comparison, recordings were also made from the specific thalamocortical relay nucleus, the ventral division of the medial geniculate body (MGv). Responses latencies were not statistically different in MGv, MGm, PIN, and SG, but were longer in the posterior thalamic region (PO). Overall, frequency tuning functions were narrower in MGv than in the other areas but many cells in MGm were as narrowly tuned as cells in MGv. There was some organization of MGv, with low frequencies represented dorsally and high frequencies ventrally. A similar but considerably weaker organization was observed in MGm. While the full range of frequencies tested (1–30 kHz) was represented in MGv, cells in MGm, PIN, and SG tended to respond best to higher frequencies (16–30 kHz). Thresholds were higher in PIN than in MGv (other areas did not differ from MGv). Nevertheless, across the various areas, the breadth of tuning was inversely related to threshold, such that more narrowly tuned cells tended to have lower thresholds. Many of the response properties observed in MGm, PIN, and SG correspond with properties found in AL neurons and thus add support to the notion that auditory responses in AL reflect thalamoamygdala transmission.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Aitkin LM (1973) Medial geniculate body of the cat: responses to tonal stimuli of neurons in medial division. J Neurophysiol 36:275–283.
Allon N, Yeshurun Y, Wollberg Z (1981) Responses of single cells in the medial geniculate body of awake squirrel monkeys. Exp Brain Res 41:222–232.
Blanchard RJ, Weiss S, Agullana R, Flores T, Blanchard DC (1991) Antipredator ultrasounds: sex differences and drug effects. Neurosci 17:818.
Bordi F, LeDoux, JE (1992) Sensory tuning beyond the sensory system: an initial analysis of auditory properties of neurons in the lateral amygdaloid nucleus and overlying areas of the striatum. J Neurosci 12 (7): 2493–2503.
Bordi F, LeDoux JE (1994) Response properties of single units in areas of rat auditory thalamus that project to the amygdala. II. Cells receiving convergent auditory and somatosensory inputs and cells antidromically activated by amygdala stimulation. Exp Brain Res 98:275–286.
Calford MB (1983) The parcellation of the medial geniculate body of the cat defined by the auditory response properties of single units. J Neurosci 3:2350–2365.
Calford MB, Aitkin LM (1983) Ascending projections to the medial geniculate body of the cat: evidence for multiple, parallel auditory pathways through thalamus. J Neurosci 3:2365–2380.
Calford MB, Webster WR (1981) Auditory representation within principal division of cat medial geniculate body: an electrophysiological study. J Neurophysiol 45:1013–1028.
Clerici WJ, Coleman JR (1990) Anatomy of the rat medial geniculate body. I. Cytoarchitecture, myeloarchitecture, and neocortical connectivity. J Comp Neurol 297:14–31.
Clugnet MC, LeDoux JE, Morrison SF (1990) Unit responses evoked in the amygdala and striatum by electrical stimulation of the medial geniculate body. J Neurosci 10:1055–1061.
Cruikshank SJ, Edeline J, Weinberger NM (1992) Stimulation at a site of auditory-somatosensory convergence in the medial geniculate nucleus is an effective unconditioned stimulus for fear conditioning. Behav Neurosci 106:471–483.
Davis M (1992) The role of the amygdala in conditioned fear. In: Aggleton JP (eds) The amygdala. Wiley-Liss, New York.
Edeline J-M (1990) Frequency-specific plasticity of single unit discharges in the rat medial geniculate body. Brain Res 529:109–119.
Edeline J-M, Weinberger NM (1991a) Thalamic short-term plasticity in the auditory system: associative retuning of receptive fields in the ventral medial geniculate body. Behav. Neurosci 105:618–635.
Edeline J-M, Weinberger NM (1991b) Subcortical adaptive filtering in the auditory system: associative retuning of receptive fields in the dorsal medial geniculate body. Behav Neurosci 105:154–175 (1991).
Edeline J-M, Weinberger NM (1992) Associative retuning in the thalamic source of input to the amygdala and auditory cortex: receptive field plasticity in the medial division of the medial geniculate body. Behav Neurosci 106:81–105.
Gross NB, Thurlow WR (1951) Microelectrode studies of neural auditory activity of cat. II. Medial geniculate body. J Neurophysiol 14:409–422.
Galambos R, Rose JE, Bromiley RB, Hughes JR (1952) Microelectrode studies on medial geniculate body of cat. II. Response to clicks. J Neurophysiol 15:359–380.
Imig TJ, Morel A (1983) Organization of the thalamocortical auditory system in the cat. Annu Rev Neurosci 6:95–120.
Jones EG, Burton H, Saper CB, Swanson LW (1976) Midbrain, diencephalic and cortical relationships of the basal nucleus of Meynert and associated structures in primates. J Comp Neurol 167:385–420.
LeDoux JE (1987) Emotion. In Plum F (eds) Higher Functions of the Brain (Handbook of physiology, sect 1, The nervous system, vol V) American Physiological Society Bethesda (1987) pp 419–460.
LeDoux JE (1992) Emotion and the amygdala. In: Aggleton JP (eds) The amygdala. Wiley-Liss New York.
LeDoux JE, Sakaguchi A, Reis DJ (1984) Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned by acoustic stimuli. J Neurosci 4(3): 683–698.
LeDoux JE, Ruggiero DA, Reis DJ (1985) Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat. J Comp Neurol 242:182–213.
LeDoux JE, Iwata J, Pearl D, Reis DJ (1986) Disruption of auditory but not visual learning by destruction of intrinsic neurons in the medial geniculate body of the rat. Brain Res 371:395–399.
LeDoux JE, Ruggiero DA, Forest R, Stornetta R, Reis DJ (1987) Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat. J Comp Neurol 264:123–146.
LeDoux JE, Farb CF, Ruggiero DA (1990a) Topographic organization of neurons in the acoustic thalamus that project to the amygdala. J Neurosci 10:1043–1054.
LeDoux JE, Cicchetti P, Xagoraris A, Romanski LM (1990b) The lateral amygdaloid nucleus: sensory interface of the amygdala in fear conditioning. J Neurosci 10:1062–1069.
LeDoux JE, Farb C, Romanski L (1991) Overlapping projections to the amygdala and striatum from auditory processing areas of the thalamus and cortex. Neurosci Lett 134:139–144.
Lennartz RC, Weinberger NM (1992) Frequency-specific receptive field plasticity in the medial geniculate body induced by Pavlovian fear conditioning is expressed in the anesthetized brain. Behav Neurosci 106:484–497.
Mehler WR (1980) Subcortical afferent connections of the amygdala in the monkey. J Comp Neurol 190:733–762.
Massopust LC, Hauge DH, Ferneding JC, Doubek WG, Taylor JJ (1985) Projection systems and terminal localization of dorsal column afferents: an autoradiographic and horseradish peroxidase study in the rat. J Comp Neurol 237:533–544.
Morel A, Rouiller E, De Ribaupierre Y, De Ribaupierre F (1987) Tonotopic organization in the medial geniculate body (MG) of lightly anesthetized cats. Exp Brain Res 69:24–42.
Morest DK (1964) The neuronal architecture of the medial geniculate body of the cat. J Anat 98:611–630.
Morest DK (1965) The lateral tegmental system of the midbrain and the medial geniculate body: study with Golgi and Nauta methods in cat. J Anat 99:611–634.
Morest DK, Winer JA (1986) The comparative anatomy of neurons. Homologous neurons in the medial geniculate body of the opossum and the cat. Adv Anat Embryol Cell Biol 97:1–96.
Møller AR (1983) Auditory physiology. Academic, New York.
Nitschke W (1982) Acoustic behavior in the rat. Praeger, New York.
Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Academic, Sydney.
Phillips DP, Irvine DR (1979) Acoustic input to single neurons in pulvinar posterior complex of cat thalamus. J Neurophysiol 42:123–136.
Romanski LM, LeDoux JE (1992) Equipotentiality of thalamoamygdala and thalamo-cortico-amygdala projections as auditory conditioned sitmulus pathways. J Neurosci 12(11): 4501–4509.
Romanski L, Clugnet MC, Bordi F, LeDoux JE (1993) Convergence of somatosensory and auditory pathways in the lateral amygdaloid nucleus: possible physiological substrate for fear conditioning Behav Neurosci 107:757–769.
Rouiller E, De Ribaupierre Y, De Ribaupierre F (1979) Phaselocked responses to low frequency tones in the medial geniculate body. Hear Res 1:213–226.
Russchen FT (1982) Amygdalopetal projections in the cat. I. Cortical afferent connections. A study with retrograde and anterograde tracing techniques. J Comp Neurol 206:159–179.
Starr A; Don M (1972) Responses of squirrel monkey (Saimiri sciureus) medial geniculate units to binaural click stimuli. J Neurophysiol 35:501–517.
Sutter ML, Schreiner CE (1991) Physiology and topography of neurons with multipeaked tuning curves in cat primary auditory cortex. J Neurophysiol 65 (5): 1207–1226.
Toros-Morel A, De Ribaupierre F, Rouiller E (1981) Coding properties of the different nuclei of the cat's medial geniculate body. In: Syka JF, Aitkin LM (eds) Neural mechanisms of hearing. Plenum, London, pp 239–243.
Walsh TM, Ebner FF (1973) Distribution of cerebellar and somatic lemniscal projections in the ventral nuclear complex of the Virginia opossum. J Comp Neurol 147:427–446.
Winer JA (1992) The functional architecture of the medial geniculate body and the primary auditory cortex. In: Webster DB, Popper AN, Fay RR (eds) The mammalian auditory pathway: Neuroanatomy. Springer, New York, pp 222–409.
Winer JA, Larue DT (1988) Anatomy of glutamic acid decarboxylase immmunoreactive neurons and axons in the rat medial geniculate body. J Comp Neurol 278:47–68.
Winer JA, Morest DK (1983) The medial division of the medial geniculate body of the cat: Implications for thalamic organization. J Neurosci 3:2629–2651.
Winer JA, Morest DK, Diamond IT (1988) A cytoarchitectonic atlas of the medial geniculate body of the opossum, Didelphys virginiana, with a comment on the posterior intralaminar nuclei of the thalamus. J Comp Neurol 274:422–448.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Bordi, F., LeDoux, J.E. Response properties of single units in areas of rat auditory thalamus that project to the amygdala. Exp Brain Res 98, 261–274 (1994). https://doi.org/10.1007/BF00228414
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00228414