{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T18:33:38Z","timestamp":1791398018805,"version":"4.3.3"},"reference-count":75,"publisher":"Wiley","issue":"5","license":[{"start":{"date-parts":[[2001,11,1]],"date-time":"2001-11-01T00:00:00Z","timestamp":1004572800000},"content-version":"vor","delay-in-days":31,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Hippocampus"],"published-print":{"date-parts":[[2001,10]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Processing of multimodal sensory information by the morphological subdivisions of the hippocampus and its input and output structures was investigated in unanesthetized rabbits by extracellular recording of neuronal activity. Analysis shows principal differences between CA3 neurons with uniform multimodal, mainly inhibitory, rapidly habituating sensory responses, and CA1\u2010subicular neurons, substantial parts of which have phasic reactions and patterned on\u2010responses, depending on the characteristics of the stimuli. These differences result from the organization of the afferent inputs to CA1 and CA3. Analysis of neuronal responses in sources of hippocampal inputs, their electrical stimulation, and chronic disconnection show the greater functional significance of the brain\u2010stem reticular input for tonic responses characteristic of CA3. This input signal before entering the hippocampus is additionally preprocessed at the MS\u2010DB relay, where it becomes more uniform and frequency\u2010modulated in the range of theta\u2010rhythm. It is shown that the new sensory stimuli produce inhibitory reset, after which synchronized theta\u2010modulation is triggered. Other stimuli, appearing at the background of the ongoing theta, do not evoke any responses of the hippocampal neurons. Thus, theta\u2010modulation can be regarded as a mechanism of attention, which prolongs response to a selected stimulus and simultaneously protects its processing against interference.<\/jats:p>\n                  <jats:p>The cortical input of the hippocampus introduces highly differentiated information analyzed at the highest levels of the neocortex through the intermediary of the entorhinal cortex and presubiculum. However, only CA1\u2010subiculum receives this information directly; before its entrance into CA3, it is additionally preprocessed at the FD relay, where the secondary simplification of signals occurs. As a result, CA3 receives by its two inputs (MS\u2010DB and FD) messages just about the presence and level of input signals in each of them, and performs relatively simple functions of determination of match\/mismatch of their weights. For this comparator system, the presence of signal only in the reticulo\u2010septal input is equivalent to quality of novelty. The cortical signal appears with some delay, after its analysis in the neocortex and shaping in the prehippocampal structures; besides, it is gradually increased due to LTP\u2010like incremental changes in PP and mossy fiber synapses. The CA3 neurons with potentiated synapses of cortical input do not respond to sensory stimuli; that is, the increased efficacy of the cortical signals can be regarded as \u201cfamiliarity\u201d of a signal, terminating the reactive state of the CA3 neurons. The integrity of both inputs is necessary for gradual habituation of sensory responses in the hippocampus.<\/jats:p>\n                  <jats:p>The output signals of CA3 following in the precommissural fornix to the output relay\u2010LS nucleus and to the brain\u2010stem structures have strong regulatory influence on the level of brain activity (arousal), which is an important condition for processing and registration of information. The primary targets of this output signal are raphe nuclei, which suppress activity of the ascending excitatory RF. In the background state, activity of the CA3 neurons through the intermediary of raphe keeps RF under tonic inhibitory control. Inhibition of the majority of CA3 pyramidal neurons during a novel stimulus action decreases the volume of its output signal to raphe and releases RF from tonic inhibition (increase in level of activity of the forebrain, arousal). When the responses of CA3 neurons habituate, the initial high background activity is reinstated, as well as tonic suppression of RF. Analysis of the second output of CA3 (by Schaffer's collaterals to CA1) shows that activity in this pathway can block access of cortical signals from PP to CA1 neurons by action upon the local system of inhibitory neurons, or by shunting the propagation of signals in apical dendrites. Thus, CA3 can act as a filter controlling the information transmission by CA1; such transmission at any given moment is allowed only in those CA1 neurons which receive SC from CA3 neurons, responding to the sensory stimulus by suppression of their activity. Disconnection of the CA3 output fibers results in disappearance of habituation in all its target structures (raphe, RF, CA1).<\/jats:p>\n                  <jats:p>The output signal of CA1\u2010subiculum follows by postcommissural fornix to the chain of structures of the main limbic circuit: mammillary bodies (medial nucleus), anterior thalamic nuclei (mainly antero\u2010ventral nucleus), and cingulate limbic cortex (mainly posterior area). In each of these links, the signal is additionally processed. Habituation is nearly absent in these structures; instead, strong incremental dynamics are observed. Various types of reaction shaping, often with changes in level and structure of background activity, are observed in them. Within this output circuit, the farther is the output structure from the hippocampus, the more repetitions of stimulus are required for shaping the sensory response. That is why this system is regarded as a chain of integrators, where each one starts to respond only after reaction develops at the previous link, and as a delay line, preventing premature fixation of spurious, irrelevant, low probability signals. The responses in the higher link of this system, the posterior limbic cortex, may be regarded as the ultimate signal for information fixation in the nonprimary areas of the neocortex. In this way, the two morpho\u2010functional circuits, regulatory (based on CA3) and informational (based on CA1), perform the unified functions of attention and initial stages of memory trace fixation. Hippocampus 2001;11:578\u2013598. \u00a9 2001 Wiley\u2010Liss, Inc.<\/jats:p>","DOI":"10.1002\/hipo.1073","type":"journal-article","created":{"date-parts":[[2004,11,14]],"date-time":"2004-11-14T06:43:44Z","timestamp":1100414624000},"page":"578-598","source":"Crossref","is-referenced-by-count":477,"title":["Hippocampus as comparator: Role of the two input and two output systems of the hippocampus in selection and registration of information"],"prefix":"10.1002","volume":"11","author":[{"given":"O.S.","family":"Vinogradova","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2001,11]]},"reference":[{"key":"e_1_2_1_2_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.92.7.2785"},{"key":"e_1_2_1_3_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0165-0173(99)00041-7"},{"key":"e_1_2_1_4_1","doi-asserted-by":"publisher","DOI":"10.1093\/schbul\/19.2.431"},{"key":"e_1_2_1_5_1","first-page":"8","volume-title":"Physiological mechanisms of memory","author":"Bragin AG","year":"1973"},{"key":"e_1_2_1_6_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF01181843"},{"key":"e_1_2_1_7_1","first-page":"249","article-title":"Analysis of non\u2010switched influences of the perforant path on the CA3 neurons in vitro","volume":"233","author":"Bragin AG","year":"1977","journal-title":"Proc Acad Sci USSR"},{"key":"e_1_2_1_8_1","first-page":"174","volume-title":"Limbic system","author":"Brazhnik ES","year":"1973"},{"key":"e_1_2_1_9_1","first-page":"1044","article-title":"Effect of septo\u2010hippocampal disconnection upon neuronal activity of the septum","volume":"25","author":"Brazhnik ES","year":"1975","journal-title":"Zh Vyssh Nerv Deiat"},{"key":"e_1_2_1_10_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF01184055"},{"key":"e_1_2_1_11_1","first-page":"1039","article-title":"Short duration synchronization of human theta rhythm during recognition memory","volume":"8","author":"Burgess AP","year":"1997","journal-title":"Neurol Rep"},{"key":"e_1_2_1_12_1","doi-asserted-by":"publisher","DOI":"10.1016\/0024-3205(87)90295-5"},{"key":"e_1_2_1_13_1","doi-asserted-by":"publisher","DOI":"10.1192\/bjp.159.6.857"},{"key":"e_1_2_1_14_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0165-0173(99)00033-8"},{"key":"e_1_2_1_15_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0006-8993(97)00575-1"},{"key":"e_1_2_1_16_1","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.95.19.11406"},{"key":"e_1_2_1_17_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0304-3940(98)00805-2"},{"key":"e_1_2_1_18_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0306-4522(98)00040-2"},{"key":"e_1_2_1_19_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0896-6273(00)80364-5"},{"key":"e_1_2_1_20_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF02900302"},{"key":"e_1_2_1_21_1","doi-asserted-by":"publisher","DOI":"10.1016\/0031-9384(70)90185-X"},{"key":"e_1_2_1_22_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0165-0173(99)00049-1"},{"key":"e_1_2_1_23_1","first-page":"1","volume-title":"Electrical activity of the archicortex","author":"Grastyan E","year":"1985"},{"key":"e_1_2_1_24_1","doi-asserted-by":"publisher","DOI":"10.1016\/0926-6410(92)90003-A"},{"key":"e_1_2_1_25_1","doi-asserted-by":"publisher","DOI":"10.1038\/4525"},{"key":"e_1_2_1_26_1","doi-asserted-by":"publisher","DOI":"10.1037\/h0026321"},{"key":"e_1_2_1_27_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF03033065"},{"key":"e_1_2_1_28_1","doi-asserted-by":"publisher","DOI":"10.1038\/21645"},{"key":"e_1_2_1_29_1","doi-asserted-by":"publisher","DOI":"10.1016\/0306-4522(90)90219-T"},{"key":"e_1_2_1_30_1","doi-asserted-by":"publisher","DOI":"10.1016\/0006-8993(70)90381-1"},{"key":"e_1_2_1_31_1","first-page":"1648","article-title":"Effects of hippocampal stimulation on neuronal activity of reticular formation","volume":"60","author":"Kitchigina VF","year":"1974","journal-title":"Physiol J USSR"},{"key":"e_1_2_1_32_1","first-page":"1266","article-title":"Significance of Schaffer's collaterals for sensory responses of the neurons in CA1 hippocampal field","volume":"25","author":"Kitchigina VF","year":"1975","journal-title":"Zh Vyssh Nerv Deiat"},{"key":"e_1_2_1_33_1","first-page":"159","article-title":"Effects of elimination of the hippocampal influences upon some midbrtain nuclei","volume":"29","author":"Kitchigina VF","year":"1979","journal-title":"Zh Vyssh Nerv Deiat"},{"key":"e_1_2_1_34_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0165-0173(98)00056-3"},{"key":"e_1_2_1_35_1","doi-asserted-by":"publisher","DOI":"10.1016\/0920-9964(94)90016-7"},{"key":"e_1_2_1_36_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0165-0173(99)00044-2"},{"key":"e_1_2_1_37_1","first-page":"51","volume-title":"Psychology of learning and motivation","author":"Miller RR","year":"1988"},{"key":"e_1_2_1_38_1","doi-asserted-by":"publisher","DOI":"10.1002\/(SICI)1098-1063(1998)8:3<212::AID-HIPO4>3.0.CO;2-L"},{"key":"e_1_2_1_39_1","first-page":"3","article-title":"The problems of inattention: methods and interpretations","volume":"38","author":"Oades RD","year":"1997","journal-title":"Behav Brain Res"},{"key":"e_1_2_1_40_1","first-page":"819","article-title":"Characteristics of neuronal reactions in limbic nuclei of thalamus. Anteroventral and anteromedial nuclei","volume":"31","author":"Pakhotin PI","year":"1981","journal-title":"Zh Vyssh Nerv Deiat"},{"key":"e_1_2_1_41_1","first-page":"1135","article-title":"Activity of the neurons of anterior thalamic nuclei after lesion of the afferent connections from hippocampus and limbic cortex","volume":"34","author":"Pakhotin PI","year":"1984","journal-title":"Zh Vyssh Nerv Deyiat"},{"key":"e_1_2_1_42_1","doi-asserted-by":"publisher","DOI":"10.1001\/archneurpsyc.1958.02340050003001"},{"key":"e_1_2_1_43_1","series-title":"The hippocampus","author":"Pribram KH","year":"1986"},{"key":"e_1_2_1_44_1","series-title":"The hippocampus","first-page":"329","author":"Pribram KH","year":"1986"},{"key":"e_1_2_1_45_1","doi-asserted-by":"publisher","DOI":"10.1037\/h0045168"},{"key":"e_1_2_1_46_1","doi-asserted-by":"publisher","DOI":"10.1055\/s-2007-999137"},{"key":"e_1_2_1_47_1","first-page":"1031","article-title":"Characteristics of neuronal activity of the ventral hippocampus","volume":"20","author":"Semyonova TP","year":"1970","journal-title":"Zh Vyssh Nerv Deiat"},{"key":"e_1_2_1_48_1","first-page":"128","article-title":"Nervous model of stimulus and the orienting reflex","volume":"4","author":"Sokolov EN","year":"1960","journal-title":"Voprosy Psichologii"},{"key":"e_1_2_1_49_1","doi-asserted-by":"publisher","DOI":"10.1037\/0033-295X.99.2.195"},{"key":"e_1_2_1_50_1","first-page":"208","volume-title":"Neural models of plasticity","author":"Squire LR","year":"1988"},{"key":"e_1_2_1_51_1","doi-asserted-by":"publisher","DOI":"10.1097\/00005053-199305000-00003"},{"key":"e_1_2_1_52_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF01182649"},{"key":"e_1_2_1_53_1","first-page":"1009","article-title":"Characteristics of neuronal activity of the hippocampal formation subdivisions. I. Subiculum","volume":"29","author":"Stafekhina VS","year":"1979","journal-title":"Zh Vyssh Nerv Deiat"},{"key":"e_1_2_1_54_1","first-page":"1276","article-title":"Characteristics of neuronal activity of the hippocampal formation subdivisions. II. Presubiculum","volume":"29","author":"Stafekhina VS","year":"1979","journal-title":"Zh Vyssh Nerv Deiat"},{"key":"e_1_2_1_55_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0304-3940(99)00726-0"},{"key":"e_1_2_1_56_1","doi-asserted-by":"publisher","DOI":"10.1615\/CritRevNeurobiol.v12.i1-2.20"},{"key":"e_1_2_1_57_1","first-page":"86","volume-title":"Orienting reflex and problems of higher neurons activity","author":"Vinogradova OS","year":"1959"},{"key":"e_1_2_1_58_1","first-page":"207","volume-title":"Orienting relations and their neurophysiological mechanisms","author":"Vinogradova OS","year":"1961"},{"key":"e_1_2_1_59_1","first-page":"1397","article-title":"Dynamic classification of the reactions of hippocampal neurons to sensory stimuli","volume":"25","author":"Vinogradova OS","year":"1966","journal-title":"Fed Proc [Neurosci Transpl]"},{"key":"e_1_2_1_60_1","first-page":"183","volume-title":"Neuronal mechanisms of the orienting reflex","author":"Vinogradova OS","year":"1975"},{"key":"e_1_2_1_61_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-1-4684-2979-4_1"},{"key":"e_1_2_1_62_1","doi-asserted-by":"publisher","DOI":"10.1016\/0301-0082(94)00051-I"},{"key":"e_1_2_1_63_1","first-page":"410","article-title":"Sensory characteristics of the hippocampal cortical input. Dentate fascia","volume":"25","author":"Vinogradova OS","year":"1975","journal-title":"Zh Vyssh Nerv Deiat"},{"key":"e_1_2_1_64_1","doi-asserted-by":"publisher","DOI":"10.1002\/9780470720394.ch8"},{"key":"e_1_2_1_65_1","first-page":"577","article-title":"Functional characteristics of the hippocampal field CA1","volume":"21","author":"Vinogradova OS","year":"1971","journal-title":"Zh Vyssh Nerv Deiat"},{"key":"e_1_2_1_66_1","first-page":"241","article-title":"On comparator function of the hippocampus","volume":"202","author":"Vinogradova OS","year":"1972","journal-title":"Proc Acad Sci USSR"},{"key":"e_1_2_1_67_1","first-page":"337","article-title":"Some properties of dynamics of nauronal activity in the limbic cortex of the rabbit","volume":"24","author":"Vinogradova OS","year":"1974","journal-title":"Zh Vyssh Nerv Deiat"},{"key":"e_1_2_1_68_1","first-page":"1260","article-title":"Sensory responses of the neurons in the medial and lateral septal nuclei","volume":"22","author":"Vinogradova OS","year":"1972","journal-title":"Zh Vyssh Nerv Deiat"},{"key":"e_1_2_1_69_1","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1016\/B978-0-12-564350-4.50021-X","volume-title":"Biology of memory","author":"Vinogradova OS","year":"1970"},{"key":"e_1_2_1_70_1","first-page":"95","article-title":"The theta modulation of rabbit hippocampal neurons and its correlation with other indices of spontaneous and evoked activity","volume":"42","author":"Vinogradova OS","year":"1992","journal-title":"Zh Vyssh Nerv Deiat Im IP Pavlova"},{"key":"e_1_2_1_71_1","doi-asserted-by":"publisher","DOI":"10.1016\/0306-4522(93)90484-W"},{"key":"e_1_2_1_72_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF01182921"},{"key":"e_1_2_1_73_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0306-4522(99)00253-5"},{"key":"e_1_2_1_74_1","series-title":"The hippocampus","first-page":"411","author":"Weiskrantz L","year":"1975"},{"key":"e_1_2_1_75_1","doi-asserted-by":"publisher","DOI":"10.1038\/17605"},{"key":"e_1_2_1_76_1","first-page":"615","article-title":"Characteristics of neuronal responses in nucleus accumbens septi to sensory stimulation","volume":"23","author":"Zolotukhina LI","year":"1973","journal-title":"Zh Vyssh Nerv Deiat"}],"container-title":["Hippocampus"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fhipo.1073","content-type":"unspecified","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/hipo.1073","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,10]],"date-time":"2023-09-10T22:50:17Z","timestamp":1694386217000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/hipo.1073"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2001,10]]},"references-count":75,"aliases":["10.1002\/hipo.1073.abs"],"journal-issue":{"issue":"5","published-print":{"date-parts":[[2001,10]]}},"alternative-id":["10.1002\/hipo.1073"],"URL":"https:\/\/doi.org\/10.1002\/hipo.1073","archive":["Portico"],"relation":{},"ISSN":["1050-9631","1098-1063"],"issn-type":[{"value":"1050-9631","type":"print"},{"value":"1098-1063","type":"electronic"}],"subject":[],"published":{"date-parts":[[2001,10]]}}}